Pancreatic cancer subtypes: a roadmap for precision medicine
Open accessAbstract
Pancreatic ductal adenocarcinoma (PDAC) is projected to become the second cause of cancer-related deaths by 2020. Although it has traditionally been approached as a disease, accumulated evidences point to the clinical heterogeneity of this disease, which translate into disparity in outcomes among the patients. Much emphasis has been put into patient classification introducing a platform for more tailored therapies. In the last 10 years, there have been important advances in the understanding of the molecular pathogenesis of PDAC, which has culminated with a comprehensive integrated genomic analysis from RNA expression profiles. Bailey et al. defined four subtypes and the different transcriptional networks underlying them. Firstly, we briefly describe and compare different subtyping approaches, which are mostly based on tissue mRNA expression analysis. We propose that these latest approaches to disease classification embrace not only those patients that are surgically resectable (20%), but even patients ineligible for surgery. Such considerations will include possible reclassification of these specific subtypes, enabling more personalized diagnosis and individualized treatment. The ultimate goal of this review is to identify current challenges in this area and summarize current efforts in developing clinical modalities that can effectively identify these subtypes in order to advance Precision Medicine. KEY MESSAGES • Pancreatic cancer can no longer be considered as one disease. • The heterogeneity underlying pancreatic cancer patients makes therapeutic options based on one-size-fits-all approach ineffective. • Identifying patients that could benefit from a specific treatment would help to avoid futile therapy approaches and to improve outcomes and quality of life of those whose long-term survival is unpromising.
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Primary tumors have been shown to undergo subtype switching in response to microenvironmental cues.
“primary tumors have been shown to undergo subtype switching in response to microenvironmental cues (Torres 2018)37.”
From Occult polyclonality of preclinical pancreatic cancer models drives in vitro evolution (2022) · cites this paper as Torres 2018
Primary tumors have been shown to undergo subtype switching in response to microenvironmental cues.
“primary tumors have been shown to undergo subtype switching in response to microenvironmental cues (Torres 2018)37.”
From Occult polyclonality of preclinical pancreatic cancer models drives in vitro evolution (2022) · cites this paper as [37]
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Occult polyclonality of preclinical pancreatic cancer models drives in vitro evolution
Monberg, M. E., Geiger, H., Lee, J. J., Sharma, R., Semaan, A., Bernard, V., Wong, J., Wang, F., Liang, S., Swartzlander, D. B., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-31376-3 · Cited by 30 · see citing works
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“having heterogeneous genetic characteristics and different biological behavior.(12,19) However, future consensus subtyping is needed to establish the subtypes relevant for clinicians.”
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“The traditional chemotherapeutic approach (one-size-fits-all) can lead to unnecessary exposure to adverse side effects without the anticipated survival benefits([96]).”
BackgroundRole of stromal activin A in human pancreatic cancer and metastasis in mice
Mancinelli, G. E., Torres, C., Krett, N. L., Bauer, J. I., Castellanos, K., McKinney, R., Dawson, D. W., Guzman, G., Hwang, R. F., Grimaldo, S., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-87213-y · Cited by 25 · see citing works
Self-citationRegulation of pancreatic cancer therapy resistance by chemokines
Gautam, S. K., Basu, S., Aithal, A., Dwivedi, N. V., Gulati, M., & Jain, M. (2022) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2022.08.010 · Cited by 25 · see citing works
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“, VEGF and VEGFR inhibitors) have been used in the clinical therapy for the benefit of patients [57], however, the treatment has no effect on a portion of patients due to the high molecular heterogeneity of PDAC [58].”
BackgroundA novel tp53-associated nomogram to predict the overall survival in patients with pancreatic cancer
Liu, X., Chen, B., Chen, J., & Sun, S. (2021) · BMC Cancer · doi:10.1186/s12885-021-08066-2 · Cited by 24 · see citing works
Understanding pancreatic cancer stem cells and their role in carcinogenesis: a narrative review
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“These genes play an important role in the early development of the pancreas via the regulation of glycosylation, fatty acid oxidation and steroid hormone/drug metabolism (7).”
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Histological variants of pancreatic ductal adenocarcinoma: a survival analysis
Bengtsson, A., Andersson, R. E., & Ansari, D. (2024) · Langenbeck s Archives of Surgery · doi:10.1007/s00423-024-03506-6 · Cited by 21 · see citing works
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“More recent developments in PDAC tumor classification include the establishment of transcriptional typing, which has emerged as the preferred method for benchmarking personalized treatment efforts [12,13].”
Translating precision medicine for autism spectrum disorder: A pressing need
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Genetics, Genomics and Emerging Molecular Therapies of Pancreatic Cancer
Liu, J., Mroczek, M., Mach, A., Stępień, M., Aplas, A., Pronobis‐Szczylik, B., Bukowski, S., Mielczarek, M., Gajewska, E., Topolski, P., et al. (2023) · Cancers · doi:10.3390/cancers15030779 · Cited by 18 · see citing works
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“A critical component of implementing PM is the judicious selection of patients who are suitable candidates for novel precision healthcare interventions [9].”
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“…that molecular sub-types can be identified in most human cancers and that different subtypes are significantly correlated with different therapeutic responses and clinical outcomes (McConkey and Choi 2018, Torres and Grippo 2018, Bozic and Wu 2020, Turajlic et al. 2020, Wolf et al. 2022).”
BackgroundTan, D. J., Mitra, M., Chiu, A. M., & Coller, H. A. (2020) · npj Genomic Medicine · doi:10.1038/s41525-020-00159-4 · Cited by 17 · see citing works
Rehman, H., Chi, J., Hakim, N., Goyal, S. P., Olazagasti, C., Jose, J., Moriarty, L., & Saif, M. W. (2020) · Therapeutic Advances in Gastroenterology · doi:10.1177/1756284820974912 · Cited by 16 · see citing works
Pancreatic stromal Gremlin 1 expression during pancreatic tumorigenesis
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“0 months survival rate).(20,26) Our study found an increase in FibroblastGrem1þ expression in all subtypes screened, with the exception of squamous, suggesting a potential significant role of FibroblastGrem1þ in PDAC development.”
Li, S., Mai, Z., Gu, W., Ogbuehi, A. C., Acharya, A., Pelekos, G., Ning, W., Liu, X., Deng, Y., Li, H., et al. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.687245 · Cited by 16 · see citing works
“Cancer precision treatment paradigm should be shifted from a biomarkers-based paradigm to a subtyping-based paradigm, and tandem research has also shifted from identification of certain critical genetic targets to detection of subtype-specific genetic targets (Dienstmann et al., 2017; Torres and Grippo, 2018; Zhao S.…”
BackgroundThe EPH/Ephrin System in Pancreatic Ductal Adenocarcinoma (PDAC): From Pathogenesis to Treatment
Papadakos, S. P., Dedes, N., Gkolemi, N., Machairas, N., & Theocharis, S. E. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24033015 · Cited by 15 · see citing works
Towards a Personalized Approach in Pancreatic Cancer Diagnostics Through Plasma Amino Acid Analysis
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Pancreatic ductal adenocarcinoma in the era of precision medicine
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Aurora kinase a inhibitor MLN8237 suppresses pancreatic cancer growth
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Involvement of CCCTC-binding factor in epigenetic regulation of cancer
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“A study showed that altered CTCF binding patterns contribute to the dysregulation of oncogenes and tumor suppressors in glioblastoma, highlighting its significance in disease development [72].”
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“Both cancer types are highly heterogeneous diseases characterized by diverse molecular and morphological features with the quasi-mesenchymal/squamous subtype of human PDAC [5] or basal-like subtype of BC [6] having the worst prognosis of any of the recently identified subtypes.”
BackgroundPalma, A. M., Vudatha, V., Peixoto, M. L., & Madan, E. (2023) · Advances in cancer research · doi:10.1016/bs.acr.2023.02.005 · Cited by 9 · see citing works
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“Although there have been some advances in precision medicine strategies for pancreas cancer, there are currently few targets for precision medicine in pancreatic tumors [33,34].”
BackgroundFei, X., Kong, L., Shi, C., Wang, G., Liu, C., Wang, C., Liu, P., & Tan, X. (2022) · Journal of Oncology · doi:10.1155/2022/7117014 · Cited by 8 · see citing works
“Previous studies have already investigated the molecular classification and the internal heterogeneity of pancreatic cancer using omics data [9, 10].”
BackgroundPancreatic adenocarcinoma and pancreatic high-grade neuroendocrine carcinoma: two sides of the moon
Salvia, A. L., Persano, I., Parlagreco, E., Audisio, A., Cani, M., & Brizzi, M. P. (2022) · Medical Oncology · doi:10.1007/s12032-022-01764-2 · Cited by 8 · see citing works
“In particular, a platinum-based firstline chemotherapy is considered the gold standard for fit patients with PDAc as well as with panNEC (Oxaliplatin in the first case and Cisplatin or Carboplatin in the second one) [59, 68].”
BackgroundInfluentialThe implication of liquid biopsies to predict chemoresistance in pancreatic cancer
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Diffuse Involvement of Pancreas is not Always Autoimmune Pancreatitis
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Ecoevolutionary biology of pancreatic ductal adenocarcinoma
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Single Cell RNA Sequencing: A New Frontier in Pancreatic Ductal Adenocarcinoma
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“Others still recommend profiling the tumor tissue of all pati nts coming in with PDAC [75] wit the recent Natio al Compre ensive Cancer Network (NCCN) guidelines for PDAC strongly recommending molecular tumor analysis [64].”
BackgroundThe road to overcome pancreatic cancer: Where are we?
Tirpe, A., Streianu, C., Isachesku, E., Şimon, I., & Berindan‐Neagoe, I. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e38196 · Cited by 6 · see citing works
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Occult polyclonality of preclinical pancreatic cancer models drives in vitro evolution
Monberg, M. E., Geiger, H. M., Lee, J. J., Sharma, R., Semaan, A., Bernard, V., Wong, J., Wang, F., Liang, S., Swartzlander, D. B., et al. (2022) · RePEc: Research Papers in Economics · Cited by 6 · see citing works
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“The response of PDAC to chemotherapy is in fl uenced by their subtypes; quasi-mesenchymal was shown to be more sensitive to gemcitabine while erlotinib was more effective in classical PDAC cell lines (Torres and Grippo, 2018).”
BackgroundSchmitt, A. M., Gätje, F. B., Tran, M. Y. R., Midelashvili, T., Xu, X., Fleischer, J. R., Spahn, H., Lai, K., Tacke, T., Younes, S., et al. (2026) · Molecular Cancer · doi:10.1186/s12943-026-02628-3 · Cited by 4 · see citing works
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“…only between a classical/pancreatic progenitor subtype, which is enriched in GNAS mutations and includes the former classical and exocrine-like subtypes [9]; and the basal-like/squamous subtype, with highly abundant TP53 mutations, consistent with the former quasi-mesenchymal subtype [10].”
BackgroundEyuboglu, S., Alpsoy, S., Uversky, V. N., & Coskuner‐Weber, O. (2024) · Computational Biology and Chemistry · doi:10.1016/j.compbiolchem.2024.108268 · Cited by 4 · see citing works
Yu, Y., Wang, Z., Mo, D. H., Wang, Z., & Li, G. (2021) · Mathematical Biosciences & Engineering · doi:10.3934/mbe.2021088 · Cited by 4 · see citing works
Gardi, N., Ketkar, M., McKinnon, R. A., Pandol, S. J., Dutt, S., & Barreto, S. G. (2021) · ANZ Journal of Surgery · doi:10.1111/ans.17194 · Cited by 4 · see citing works
Pedrosa, L., Araujo, I. K., Cuatrecasas, M., Soy, G., López‐Prades, S., Maurel, J., Sánchez-Montes, C., Montironi, C., Saurí, T., Sendino, O., et al. (2023) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2023.1161893 · Cited by 4 · see citing works
“Among different levels of omic datasets, transcriptomic data has been successfully applied to respond to clinical questions for prognosis stratification and therapeutic decisions (Torres and Grippo, 2018; Turanli et al., 2021).”
BackgroundEpigenetic therapeutic strategies in pancreatic cancer
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Optical phenotyping using label-free microscopy and deep learning
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“Based on the molecular alteration, PDAC can be classi fi ed into four major classes, namely squamous subtype, progenitor subtype, immunogenic subtype, and aberrantly differentiated endocrine subtype [6].”
Baloyan, E., Zohrabyan, D., Safaryan, L., Avagyan, A., Harutyunyan, L., Bardakhchyan, V. G., Arakelyan, J., Sargsyan, A., Harutyunyan, M., Mailyan, M., et al. (2025) · JCO Global Oncology · doi:10.1200/go.24.00217 · Cited by 3 · see citing works
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THE INNOVATIONS, ADVANCES AND OUTLOOKS OF LIQUID BIOPSY IN ONCOLOGY: A LITERATURE REVIEW
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InfluentialUnlocking the Pancreatic Cancer Puzzle: Using Intermediate Cells to Target Treatment
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“In pancreatic tumors, spatially varying cellular composition and microenvironmental structure give rise to phenotypes that correlate with clinical outcome [2].”
- Authors
- Torres, C., & Grippo, P. J.
- Affiliations
- University of Illinois Chicago (US)
- Corresponding author
- Torres, Carolina
- Venue
- Annals of Medicine
- Publisher
- Informa UK Limited
- Published
- 2018-03-22
- Volume
- 50
- Issue
- 4
- Pages
- 277-287
- ISSN
- 0785-3890 (ISSN-L)
- 1365-2060
- PMC
- PMC6151873
- OpenAlex
- W2793975714
- Cited by
- 104
- References
- 54
- Citations by year
- 2026: 10 · 2025: 8 · 2024: 11 · 2023: 16 · 2022: 21 · 2021: 20 · 2020: 9 · 2019: 7 · 2018: 2
- FWCI
- 1.05
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Annals of Medicine (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH (1R01CA161283)
- Topics
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Breast Cancer Treatment Studies
- Keywords
- pancreatic ductal adenocarcinoma, tumor subtypes, molecular classification, precision medicine, RNA expression profiling, tumor heterogeneity, personalized treatment, resectability, unresectable pancreatic cancer
- MeSH terms
- Antineoplastic Combined Chemotherapy Protocols, Clinical Trials as Topic, Humans, Pancreas, Pancreatectomy, Pancreatic Neoplasms, Prognosis, RNA, Messenger, Biomarkers, Tumor, Treatment Outcome, Patient Selection, Drug Resistance, Neoplasm, Gene Expression Profiling, Carcinoma, Pancreatic Ductal, Genomics, Precision Medicine, Molecular Targeted Therapy
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