The urokinase plasminogen activator system: a target for anti-cancer therapy

Ulisse, Salvatore; Baldini, Enke; Sorrenti, Salvatore; D'Armiento, Massimino

doi:10.2174/156800909787314002

Cited by 322Protease and Inhibitor MechanismsBlood Coagulation and Thrombosis MechanismsTGF-β signaling in diseases

The urokinase plasminogen activator system: a target for anti-cancer therapy

Ulisse, Salvatore, Baldini, Enke, Sorrenti, Salvatore, D'Armiento, Massimino·2009·Current Cancer Drug Targets

DOI 10.2174/156800909787314002

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Abstract

The urokinase plasminogen activator (uPA) system (uPAS) consists of the uPA, its cognate receptor (uPAR) and two specific inhibitors, the plasminogen activator inhibitor 1 (PAI-1) and 2 (PAI-2). The uPA converts the proenzyme plasminogen in the serine protease plasmin, involved in a number of physiopathological processes requiring basement membrane (BM) and/or extracellular matrix (ECM) remodelling, including tumor progression and metastasis. Data accumulated over the past years have made increasingly clear that the uPAS has a multifunctional task in the neoplastic evolution, affecting tumor angiogenesis, malignant cell proliferation, adhesion and migration, intravasation and growth at the metastatic site. In agreement with their role in cancer progression and metastasis, an increased expression of uPA, uPAR, and PAI-1 has been documented in several malignant tumors, and a positive correlation between the levels of one or more uPAS members and a poor prognosis has been frequently reported. This is particularly evident in breast cancer, for which uPA has been demonstrated to be the most potent independent prognostic factor described to date. The involvement of the uPAS in cancer progression identifies its components as suitable targets for anti-cancer therapy. Several therapeutical approaches aimed at inhibiting the uPA/uPAR functions have been shown to possess anti-tumor effects in xenograft models, including selective inhibitors of uPA activity, antagonist peptides, monoclonal antibodies able to prevent uPA binding to uPAR and gene therapy techniques silencing uPA/uPAR expression. All these strategies, however, although promising, need definitive confirmation in humans as, up to now, only few uPA inhibitors entered clinical trial.

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Expression of PAI-1 is linked to poor outcome in breast cancer.
“For example, the plasminogen system has been linked to cancer with expression of PAI-1 linked to poor outcome in breast cancer (70).”
From Diabetes and Cancer (2010) · cites this paper as [70]

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Diabetes and Cancer
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Multifaceted Role of the Urokinase-Type Plasminogen Activator (uPA) and Its Receptor (uPAR): Diagnostic, Prognostic, and Therapeutic Applications
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Tumor-Specific Activation of an EGFR-Targeting Probody Enhances Therapeutic Index
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Polymer Nanoparticles Mediated Codelivery of AntimiR-10b and AntimiR-21 for Achieving Triple Negative Breast Cancer Therapy
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The role of tumor-associated macrophages in breast cancer progression
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Ten-year analysis of the prospective multicentre Chemo-N0 trial validates American Society of Clinical Oncology (ASCO)-recommended biomarkers uPA and PAI-1 for therapy decision making in node-negative breast cancer patients
Harbeck, N., Schmitt, M., Meisner, C., Friedel, C., Untch, M., Schmidt, M., Sweep, F. C. G. J., Lisboa, B., Lux, M. P., Beck, T., et al. (2013) · European Journal of Cancer · doi:10.1016/j.ejca.2013.01.007 · Cited by 169 · see citing works
Cannabidiol inhibits angiogenesis by multiple mechanisms
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uPA/uPAR and SERPINE1 in head and neck cancer: role in tumor resistance, metastasis, prognosis and therapy
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Cannabidiol, a non-psychoactive cannabinoid compound, inhibits proliferation and invasion in U87-MG and T98G glioma cells through a multitarget effect
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Diabetes and Risk of Cancer
Habib, S. L., & Rojna, M. (2013) · ISRN Oncology · doi:10.1155/2013/583786 · Cited by 128 · see citing works
Role of Urokinase Receptor in Tumor Progression and Development
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VEGF-initiated angiogenesis and the uPA/uPAR system
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Enzyme targeting strategies for prevention and treatment of cancer: Implications for cancer therapy
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Apigenin: A natural bioactive flavone-type molecule with promising therapeutic function
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Masked Chimeric Antigen Receptor for Tumor-Specific Activation
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Targeting of surface alpha-enolase inhibits the invasiveness of pancreatic cancer cells
Principe, M., Ceruti, P., Shih, N., Chattaragada, M. S., Rolla, S., Conti, L., Bestagno, M., Zentilin, L., Yang, S., Migliorini, P., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.3572 · Cited by 110 · see citing works
Papillary Thyroid Cancer Prognosis: An Evolving Field
Ulisse, S., Baldini, E., Lauro, A., Pironi, D., Tripodi, D., Lori, E., Ferent, I. C., Amabile, M. I., Catania, A., Matteo, F. M. D., et al. (2021) · Cancers · doi:10.3390/cancers13215567 · Cited by 110 · see citing works
uPAR promotes tumor-like biologic behaviors of fibroblast-like synoviocytes through PI3K/Akt signaling pathway in patients with rheumatoid arthritis
Liu, Y., Pan, Y., Xue, Y.-Q., Fang, L., Guo, X.-H., Guo, X., Liu, M., Mo, B., Yang, M.-R., Liu, F., et al. (2017) · Cellular and Molecular Immunology · doi:10.1038/cmi.2016.60 · Cited by 107 · see citing works
Matrix Metalloproteinase-9 Regulates Tumor Cell Invasion through Cleavage of Protease Nexin-1
Xu, D., McKee, C. M., Cao, Y., Ding, Y., Kessler, B. M., & Muschel, R. J. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-0242 · Cited by 102 · see citing works
MicroRNA-182 drives metastasis of primary sarcomas by targeting multiple genes
Sachdeva, M., Mito, J. K., Lee, C., Zhang, M., Li, Z., Dodd, R. D., Cason, D., Luo, L., Ma, Y., Mater, D. V., et al. (2014) · Journal of Clinical Investigation · doi:10.1172/jci77116 · Cited by 95 · see citing works
Cancer therapy trials employing level-of-evidence-1 disease forecast cancer biomarkers uPA and its inhibitor PAI-1
Schmitt, M., Harbeck, N., Brünner, N., Jänicke, F., Meisner, C., Muehlenweg, B., Jansen, H., Dorn, J., Nitz, U. A., Kantelhardt, E. J., et al. (2011) · Expert Review of Molecular Diagnostics · doi:10.1586/erm.11.47 · Cited by 95 · see citing works
Enhanced cell migration and apoptosis resistance may underlie the association between high SERPINE1 expression and poor outcome in head and neck carcinoma patients
Pavón, M. Á., Arroyo‐Solera, I., Gabriel, M. T., León, X., Porcuna, D. V., López, M., Gallardo, A., Céspedes, M. V., Casanova, I., Pousa, A. L., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.5032 · Cited by 91 · see citing works
Lycopene inhibits angiogenesis both in vitro and in vivo by inhibiting MMP ‐2/u PA system through VEGFR 2‐mediated PI 3 K ‐ A kt and ERK /p38 signaling pathways
Chen, M., Lin, Y., Yang, C., & Hu, M. (2012) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201100683 · Cited by 91 · see citing works
FOXM1c Promotes Pancreatic Cancer Epithelial-to-Mesenchymal Transition and Metastasis via Upregulation of Expression of the Urokinase Plasminogen Activator System
Huang, C., Xie, D., Cui, J., Li, Q., Gao, Y., & Xie, K. (2014) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-2311 · Cited by 87 · see citing works
Chromosomal, epigenetic and microRNA-mediated inactivation of LRP1B, a modulator of the extracellular environment of thyroid cancer cells
Prazeres, H., Torres, J., Rodrigues, F., Pinto, M. T., Pastoriza, M. C., Gomes, D., Cameselle‐Teijeiro, J., Vidal, A., Martins, T., Sobrinho-Simões, M. A., et al. (2010) · Oncogene · doi:10.1038/onc.2010.512 · Cited by 87 · see citing works
Erratum: Chromosomal, epigenetic and microRNA-mediated inactivation of LRP1B, a modulator of the extracellular environment of thyroid cancer cells
Prazeres, H., Torres, J., Rodrigues, F., Pinto, M. T., Pastoriza, M. C., Gomes, D., Cameselle‐Teijeiro, J., Vidal, A., Martins, T., Sobrinho-Simões, M. A., et al. (2016) · Oncogene · doi:10.1038/onc.2016.143 · Cited by 85 · see citing works
Phase II randomised proof-of-concept study of the urokinase inhibitor upamostat (WX-671) in combination with gemcitabine compared with gemcitabine alone in patients with non-resectable, locally advanced pancreatic cancer
Heinemann, V., Ebert, M. P., Laubender, R. P., Bevan, P., Mala, C., & Boeck, S. H. (2013) · British Journal of Cancer · doi:10.1038/bjc.2013.62 · Cited by 82 · see citing works
A Statistics-based Platform for Quantitative N-terminome Analysis and Identification of Protease Cleavage Products
Keller, U. A. D., Prudova, A., Gioia, M., Butler, G. S., & Overall, C. M. (2010) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m000032-mcp201 · Cited by 81 · see citing works
Structure–Activity Relationship of Benzofuran Derivatives with Potential Anticancer Activity
Farhat, J., Alzyoud, L., Alwahsh, M., & Al‐Omari, B. (2022) · Cancers · doi:10.3390/cancers14092196 · Cited by 79 · see citing works
Role of angiogenesis in melanoma progression: Update on key angiogenic mechanisms and other associated components
Cho, W. C., Jour, G., & Aung, P. P. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.06.015 · Cited by 83 · see citing works
Evodiamine induces apoptosis and inhibits metastasis in MDA-MB-231 human breast cancer cells in vitro and in vivo
Du, J., Wang, X., Zhou, Q., ZHANG, T.-L., Lu, Y.-Y., Zhang, H., & Su, S.-B. (2013) · Oncology Reports · doi:10.3892/or.2013.2498 · Cited by 76 · see citing works
Structural Basis for Recognition of Urokinase-type Plasminogen Activator by Plasminogen Activator Inhibitor-1
Lin, Z., Jiang, L., Yuan, C., Jensen, J. K., Zhang, X., Luo, Z., Furie, B. C., Furie, B., Andreasen, P. A., & Huang, M. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.204537 · Cited by 73 · see citing works
Modulators of the urokinase-type plasminogen activation system for cancer
Hildenbrand, R., Allgayer, H., Marx, A., & Ströbel, P. (2010) · Expert Opinion on Investigational Drugs · doi:10.1517/13543781003767400 · Cited by 71 · see citing works
Identification and pre-clinical testing of a reversible cathepsin protease inhibitor reveals anti-tumor efficacy in a pancreatic cancer model
Elie, B. T., Gocheva, V., Shree, T., Dalrymple, S. A., Holsinger, L. J., & Joyce, J. A. (2010) · Biochimie · doi:10.1016/j.biochi.2010.04.023 · Cited by 69 · see citing works
Extracellular Matrix: Emerging Roles and Potential Therapeutic Targets for Breast Cancer
Zhao, Y., Zheng, X., Zheng, Y., Chen, Y., Fei, W., Wang, F., & Zheng, C. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.650453 · Cited by 72 · see citing works
uPAR-expressing melanoma exosomes promote angiogenesis by VE-Cadherin, EGFR and uPAR overexpression and rise of ERK1,2 signaling in endothelial cells
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Lithocholic acid upregulates uPAR and cell invasiveness via MAPK and AP-1 signaling in colon cancer cells
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6-Substituted Hexamethylene Amiloride (HMA) Derivatives as Potent and Selective Inhibitors of the Human Urokinase Plasminogen Activator for Use in Cancer
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Authors: Ulisse, S., Baldini, E., Sorrenti, S., & D'Armiento, M.
Affiliations: Sapienza University of Rome (IT)
ORCID: Ulisse, Salvatore
Baldini, Enke
Sorrenti, Salvatore
Venue: Current Cancer Drug Targets
Publisher: Bentham Science Publishers Ltd.
Published: 2009-02-01
Volume: 9
Issue: 1
Pages: 32-71
ISSN: 1568-0096 (ISSN-L)
DOI: 10.2174/156800909787314002
OpenAlex: W2135351121
Cited by: 312
References: 493
Citations by year: 2026: 6 · 2025: 6 · 2024: 8 · 2023: 8 · 2022: 16 · 2021: 18 · 2020: 14 · 2019: 16 · 2018: 16 · 2017: 17 · 2016: 17 · 2015: 23 · 2014: 33 · 2013: 31 · 2012: 25
FWCI: 9.37
Type: journal article
Language: en
Open access: closed
Locations: Current Cancer Drug Targets (publishedVersion)
PubMed (publishedVersion)
IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Protease and Inhibitor Mechanisms
Health Sciences › Medicine › Hematology › Blood Coagulation and Thrombosis Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
Keywords: urokinase, urokinase receptor, plasminogen activator inhibitor-1, plasminogen activator inhibitor-2, plasmin, extracellular matrix remodeling, metastasis, tumor progression, tumor angiogenesis, breast cancer, prognostic factors, cancer therapy, uPA inhibitors, monoclonal antibodies, gene therapy, xenograft models
MeSH terms: Antineoplastic Agents, Humans, Neoplasms, Urokinase-Type Plasminogen Activator

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The urokinase plasminogen activator system: a target for anti-cancer therapy

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