Targeting DNA damage repair pathways in pancreas cancer

Crowley, Fionnuala; Park, Wungki; O’Reilly, Eileen M.

doi:10.1007/s10555-021-09983-1

Cited by 44Pancreatic and Hepatic Oncology ResearchPARP inhibition in cancer therapyCancer Genomics and Diagnostics

Targeting DNA damage repair pathways in pancreas cancer

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Crowley, Fionnuala, Park, Wungki, O’Reilly, Eileen M.·2021·Cancer and Metastasis Reviews

DOI 10.1007/s10555-021-09983-1PMC PMC9391023

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Abstract

Pancreas ductal adenocarcinoma (PDAC) is the third most common cause of cancer death in the USA. While other cancers with historically poor prognoses have benefited from new immunotherapies and targeted agents, the 5-year survival rate for PDAC patients has remained static. The accessibility to genomic testing has improved in recent years, and it is now clear that PDAC is a heterogenous disease, with a subset of patients harboring actionable mutations. There are several targeted therapies approved by the Food and Drug administration (FDA) in PDAC: EGFR inhibitor erlotinib (combined with gemcitabine) in unselected patients, TRK inhibitors larotrectinib and entrectinib for patients with NTRK fusion mutation, the PD-1 inhibitor pembrolizumab for mismatch repair-deficient patients, and the poly-ADP-ribose polymerase (PARP) inhibitor olaparib in patients with germline BRCA mutation as a maintenance therapy. DNA damage repair (DDR) is paramount to genomic integrity and cell survival. The defective repair of DNA damage is one of the hallmarks of cancer, and abnormalities in DDR pathways are closely linked with the development of malignancies and upregulation of these pathways linked with resistance to treatment. The prevalence of somatic and germline mutations in DDR pathways in metastatic PDAC is reported to be approximately 15-25%. Patients with DDR gene alterations benefit from a personalized approach to treatment. Recently, the POLO trial demonstrated a progression-free survival (PFS) benefit in metastatic PDAC patients with a germline BRCA1/2 mutation treated with maintenance olaparib following platinum-based induction chemotherapy. This was the first phase 3 randomized trial to establish a biomarker-driven approach in the treatment of PDAC and establishes a precedent for maintenance therapy in PDAC. The review herein aims to outline the current treatment landscape for PDAC patients with DDR gene-mutated tumors, highlight novel therapeutic approaches focused on surmounting tumor resistance, and explore new strategies which may lead to an expansion in the number of patients who benefit from these targeted treatments.

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The ATM-TP53 signaling pathway is critical in DDR targeting in pancreatic cancer.
“The ATM-TP53 signaling pathway is critical in DDR targeting in pancreatic cancer70.”
From Impact of KRAS mutations and co-mutations on clinical outcomes in pancreatic ductal adenocarcinoma (2024) · cites this paper as [70]

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Rucaparib Monotherapy in Patients With Pancreatic Cancer and a Known Deleterious BRCA Mutation
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Genomic Features and Classification of Homologous Recombination Deficient Pancreatic Ductal Adenocarcinoma
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mTOR Inhibitors Suppress Homologous Recombination Repair and Synergize with PARP Inhibitors via Regulating SUV39H1 in BRCA-Proficient Triple-Negative Breast Cancer
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Doubling Down on the PI3K-AKT-mTOR Pathway Enhances the Antitumor Efficacy of PARP Inhibitor in Triple Negative Breast Cancer Model beyond BRCA-ness
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Immunotherapy in pancreatic ductal adenocarcinoma: an emerging entity?
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Prevalence of BRCA1 and BRCA2 mutations in Ashkenazi Jewish families with breast and pancreatic cancer
Stadler, Z. K., Salo‐Mullen, E. E., Patil, S. M., Pietanza, M. C., Vijai, J., Saloustros, E. S., Hansen, N. A. L., Kauff, N. D., Kurtz, R. C., Kelsen, D. P., et al. (2011) · Cancer · doi:10.1002/cncr.26191 · Cited by 98 · see citing works
Molecular landscape of pancreatic cancer: implications for current clinical trials
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Phase II study of olaparib + durvalumab (MEDIOLA): Updated results in germline BRCA-mutated platinum-sensitive relapsed (PSR) ovarian cancer (OC)
Drew, Y., Kaufman, B., Banerjee, S. N., Lortholary, A. H., Hong, S. H., Park, Y. H., Zimmermann, S., Roxburgh, P., Ferguson, M., Álvarez, R. H., et al. (2019) · Annals of Oncology · doi:10.1093/annonc/mdz253.016 · Cited by 96 · see citing works
Antitumor effect of a WEE1 inhibitor and potentiation of olaparib sensitivity by DNA damage response modulation in triple-negative breast cancer
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Overall survival from the phase 3 POLO trial: Maintenance olaparib for germline BRCA-mutated metastatic pancreatic cancer.
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Olaparib in combination with irinotecan, cisplatin, and mitomycin C in patients with advanced pancreatic cancer
Yarchoan, M. M., Myzak, M. C., Johnson, B. A., Jesus‐Acosta, A. D., Le, D. T., Jaffee, E. M., Azad, N. S., Donehower, R. C., Zheng, L., Oberstein, P. E., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.17237 · Cited by 77 · see citing works
Geographic and Ethnic Heterogeneity of Germline BRCA1 or BRCA2 Mutation Prevalence Among Patients With Metastatic Pancreatic Cancer Screened for Entry Into the POLO Trial
Golan, T., Kindler, H. L., Park, J. O., Reni, M., Macarulla, T. M., Hammel, P. R., Cutsem, E. V., Arnold, D., Hochhauser, D., McGuinness, D. H., et al. (2020) · Journal of Clinical Oncology · doi:10.1200/jco.19.01890 · Cited by 73 · see citing works
Association between homologous recombination repair gene mutations and response to oxaliplatin in pancreatic cancer
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High Prevalence of BRCA1 and BRCA2 Germline Mutations with Loss of Heterozygosity in a Series of Resected Pancreatic Adenocarcinoma and Other Neoplastic Lesions
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A phase III study comparing single-agent olaparib or the combination of cediranib and olaparib to standard platinum-based chemotherapy in recurrent platinum-sensitive ovarian cancer.
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Efficacy of platinum-based chemotherapy and prognosis of patients with pancreatic cancer with homologous recombination deficiency: comparative analysis of published clinical studies
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A Phase I/II Study of Veliparib (ABT-888) in Combination with 5-Fluorouracil and Oxaliplatin in Patients with Metastatic Pancreatic Cancer
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Phase IB trial of cisplatin (C), gemcitabine (G), and veliparib (V) in patients with known or potential BRCA or PALB2-mutated pancreas adenocarcinoma (PC).
O'Reilly, E. M., Lowery, M. A., Segal, M. F., Smith, S., Moore, M. J., Kindler, H. L., Golan, T., Segal, A., Salo‐Mullen, E. E., Hollywood, E. M., et al. (2014) · Journal of Clinical Oncology · doi:10.1200/jco.2014.32.15_suppl.4023 · Cited by 34 · see citing works
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Randomized phase II study of second-line modified FOLFIRI with PARP inhibitor ABT-888 (Veliparib) (NSC-737664) versus FOLFIRI in metastatic pancreatic cancer (mPC): SWOG S1513.
Chiorean, E. G., Guthrie, K. A., Philip, P. A., Swisher, E. M., Jalikis, F. G., Pishvaian, M. J., Berlin, J., Noel, M. S., Suga, J. M., Garrido‐Laguna, I., et al. (2019) · Journal of Clinical Oncology · doi:10.1200/jco.2019.37.15_suppl.4014 · Cited by 32 · see citing works
Abstract CT234: A Phase II, single arm study of maintenance rucaparib in patients with platinum-sensitive advanced pancreatic cancer and a pathogenic germline or somatic mutation in BRCA1, BRCA2 or PALB2
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Phase III PAOLA-1/ENGOT-ov25 trial: Olaparib plus bevacizumab (bev) as maintenance therapy in patients (pts) with newly diagnosed, advanced ovarian cancer (OC) treated with platinum-based chemotherapy (PCh) plus bev
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Germline BRCA mutations in Asian patients with pancreatic adenocarcinoma: a prospective study evaluating risk category for genetic testing
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The Interaction of PI3K Inhibition with Homologous Recombination Repair in Triple Negative Breast Cancer Cells
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PARP Inhibition Combined with Immune Checkpoint Blockade in SCLC: Oasis in an Immune Desert or Mirage?
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Targeting DNA Damage Repair Pathways in Pancreatic Adenocarcinoma
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The role of PARP inhibitors in germline BRCA-associated pancreatic ductal adenocarcinoma.
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Oral-antral fistulas: a review.
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Impact of KRAS mutations and co-mutations on clinical outcomes in pancreatic ductal adenocarcinoma
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Clinico-genomic Characterization of ATM and HRD in Pancreas Cancer: Application for Practice
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Targeting CLK1/SRSF7 axis-dependent alternative splicing sensitizes pancreatic ductal adenocarcinoma to chemotherapy and immunotherapy
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Enhancing the anti-tumor response by combining DNA damage repair inhibitors in the treatment of solid tumors
Yu, X., Zhu, L., Wang, T., Li, L., Liu, J., Che, G., & Zhou, Q. (2023) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2023.188910 · Cited by 14 · see citing works
Detection and therapeutic implications of homologous recombination repair deficiency in pancreatic cancer: a narrative review
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Exploring epigenetic dynamics unveils a super-enhancer-mediated NDRG1-β-catenin axis in modulating gemcitabine resistance in pancreatic cancer
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Authors: Crowley, F., Park, W., & O’Reilly, E. M.
Affiliations: Mount Sinai Hospital (US)
Memorial Sloan Kettering Cancer Center (US)
ORCID: Crowley, Fionnuala
Park, Wungki
O’Reilly, Eileen M.
Venue: Cancer and Metastasis Reviews
Publisher: Springer Science and Business Media LLC
Published: 2021-08-17
Volume: 40
Issue: 3
Pages: 891-908
ISSN: 0167-7659 (ISSN-L)
1573-7233
DOI: 10.1007/s10555-021-09983-1
PMC: PMC9391023
OpenAlex: W3194003153
Cited by: 43
References: 127
Citations by year: 2026: 6 · 2025: 11 · 2024: 6 · 2023: 12 · 2022: 5 · 2021: 3
FWCI: 0.79
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Cancer and Metastasis Reviews (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Cancer Institute (P30CA008748, K12CA184746)
Topics: Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
Health Sciences › Medicine › Oncology › PARP inhibition in cancer therapy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
Keywords: pancreatic ductal adenocarcinoma, DNA repair, PARP inhibitors, olaparib, BRCA mutations, germline mutations, targeted therapy, treatment resistance, maintenance therapy, mismatch repair deficiency, NTRK fusion, EGFR inhibitors, pembrolizumab, biomarker-driven treatment
MeSH terms: Poly(ADP-ribose) Polymerase Inhibitors, DNA Damage, DNA Repair, Humans, Pancreatic Neoplasms, Carcinoma, Pancreatic Ductal

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