The Tumor Proteolytic Landscape: A Challenging Frontier in Cancer Diagnosis and Therapy
Abstract
:1. Introduction
2. Proteases in the Tumor Microenvironment
2.1. Metalloproteases
2.2. Serine Proteases
2.3. Cysteine Proteases
2.4. Aspartic Proteases
2.5. Threonine Proteases
3. Monitoring Protease Activity in Cancer
3.1. Activity- and Substrate-Based Probes
3.2. Integrating In Vivo Imaging Modalities
3.3. New Developments and Trends
4. Leveraging Protease Activity in Drug Delivery for Cancer Therapy
4.1. Prodrugs
4.2. Antibody Drugs
4.3. Polymers
4.4. Liposomes
4.5. Inorganic Nanomaterials
5. Conclusions and Outlook
Author Contributions
Funding
Conflicts of Interest
References
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Cancer Hallmark | Example Proteases and Protease Groups | Mechanistic Roles, Functions and Consequences | Selected References |
---|---|---|---|
Cancer cell proliferation | MMP2, 3, ADAM10, 17 Cathepsins Kallikreins | ECM remodeling, signaling, processing of growth factors, sustain and boost proliferative signaling pathways | [33,34,35,36] [18,37] [38,39] |
Resisting cell death | MMP7, ADAM10 Granzyme B HtrA Caspases Cathepsins B, L, S Cathepsin D | Apoptosis signaling, apoptosis resistance, circumvent apoptosis triggers, autophagy recycling, immune system evasion | [22,40] [41,42] [43] [44,45] [18,37] [46] |
Evading growth suppressor signals | Various MMPs and ADAMs ADAMTs Kalikreins, Cathepsins | Cytokine and chemokine secretion, removal of cellular brakes, receptor signaling, disruption of p53 signaling | [22,36,40,47,48] [49,50,51] [39,52,53] [54,55] |
Support replicative immortality | Multiple MMPs ADAM10, 17 Granyzme B Cathepsins B, L, S KLK4-7 | Sustain growth signaling, release of biologically active fragments, immune system evasion, immune system hijacking | [33,56,57] [36,47,48] [41,42] [37,54,58,59] [60] |
Angiogenesis and neovascularization | MMP1, 2, 9 Kallikreins PSA Cathepsins B, L, K, S Calpains | Growth factor signaling, ECM remodeling, degradation of structural proteins, release of cytokines, receptor shedding | [61,62,63] [52,53] [64] [37,54,59,65] [66,67] |
Metastasis and invasion | MMP1, 14 ADAM10, 17 Kalikreins Cathepsin G PSA FAP, DPPIV, PEP Cathepsins B, L, K, S Legumain Cathepsin D, E Calpains | ECM remodeling, barrier degradation, cancer cell migration, receptor signaling, metabolic signaling, epithelial-to mesenchymal transition, release and modulation of signaling molecules, kinase signaling perturbation | [61,62,63] [36,47,48] [52,53] [68,69] [64] [70] [37,54,58,59] [71] [46,72] [73,74] |
Protease-Responsive Nanodevices | Application Notes (+ Advantages, − Shortcomings) | Selected Examples and References |
---|---|---|
Activity-based probes | + Sensitive detection of proteases in situ in cells and animal models + Excellent selectivity for target proteases − No signal amplification | Metalloproteases [213,214,215], serine proteases [216] including neutrophil proteases [217] and inflammation-related serine proteases [218], cysteine cathepsins [219,220], caspases [221,222] and legumain [223,224], aspartic proteases [225], and proteasome [226,227] |
Protease-cleavable fluorescent substrate probes | + Signal amplification + Selectivity can be improved by designs that incorporate unnatural amino acids − Background fluorescence and signal diffusion | Profiling of caspases [222], cathepsins [238,239], neutrophil proteases [217] and kallikreins [240] |
QDs | + Sensitivity of integrated FRET + Versatile platform − Toxicity of nanoparticles | Imaging and detection MMPs [247,248], caspase-1, collagenase, chymotrypsin and thrombin [249], uPAR [250], caspase-3 [251] and kallikrein [252] |
PET and SPECT probes | + High sensitivity and resolution − Short half-life of reagents because of radioactive isotopes − Costly detection modalities | Protease-responsive contrast agents for metalloproteases [263,264,265], cysteine cathepsins [266,267,268] and caspases [269,270] |
MRI probes | + High sensitivity and resolution for soft tissues − Expensive detection modality | MMP-2 in tumors [274], caspase activity after drug-induced apoptosis [275], caspase-3 [276], digestive elastases [277], cysteine cathepsins [279] and furin [280] |
CT probes | + Resolution for in-depth tissue imaging − Lack of suitable protease-sensitive probes | Protease-targeted iodinated probe [272] and protease activity probes with gold nanoparticles [273] were for cysteine cathepsins |
Dual modality probes | + Improved spatiotemporal resolution and sensitivity − Expensive and do not overcome the problems of original modalities | NIR/PET probes sensitive for MMP-2, MMP-9, and MMP-13 [281], FRET/SPECT probe for MMP-2 [282] and a FRET/MRI probe for MMP-2 [283] |
DARPins | + Selectivity for target protease + Can be integrated with other modalities − Intensive development and selection process | Imaging of cathepsin B in breast cancer [288] |
Synthetic biomarkers | + Sensitive in situ detection of protease activity + High multiplexing capabilities − Not best-suited for on-site monitoring (i.e., imaging) | Colorectal cancer biomarker detection in plasma [289], magnetically actuated protease sensors (MAPS) for measuring MMP tumor profiles in colorectal cancer [290], activity-based nanosensors (ABNs) for MMP-9 [291], Ultra small gold nanoclusters (AuNC) as MMP-responsive nanosensors [292], prostate cancer nanosensors [293] and lung cancer nanosensors [294] |
Prodrugs with protease-cleavable linkers | + Protease-dependent on-site activation − Off-site drug release due to unspecific protease cleavage | Legumain-sensitive Ala-Ala-Asn linker [303], cathepsin B-sensitive linker Val-Cit [304] and prodrugs that require metalloproteases, kallikreins, cathepsins or coagulation proteases [305] |
Ab-drug conjugates | + Improved on-site targeting of the drug − Problems with selective cancer cell recognition | ADCERTIS [308] and Polivy [309] |
Probody | + Protease-dependent on-site activation of the Ab − Non-selective peptide linker cleavage | EGFR targeting probody activated by legumain, uPA or matriptase cleavage from CytomX Therapeutics [311] |
Polymers | + Favorable biologic properties of polymers + Accumulation on target site due to EPR effect + Selective on-site release of polymer-bound drug by the target protease − Prolonged retention and off-site accumulation − Non-selective protease degradation of the polymers − Anti-polymer antibodies arise in patients | PEG-functionalized MMP-2-sensitive QDs clusters [320], MMP-2-sensitive PEG 2000-paclitaxel conjugate [321], SELPs (Silk-elastin-like protein polymers) polymers as MMP-responsive delivery agents [322], cathepsin B sensitive poly(L-glutamic acid)-paclitaxel conjugate [323] as well thrombin-sensitive [324] and trypsin-sensitive [325] conjugates, a PSA-sensitive HPMA-thapsigargin conjugate [326] |
Liposomes | + Small size and favorable biological properties + Can be integrated with various other modalities − Accelerated clearance from cardiovascular system − Potential for allergic reactions | PEGylated MMP-sensitive lyposome [330], polymer-caged uPA-sensitive liposomes [331], PEGylated liposome with a MMP-cleavable lipopeptide [332], TAT peptide bearing legumain-activated liposome [333], a MMP-9-sensitive ‘uncorking’ liposome [334], a cathepsin B targeting liposome [335] |
Inorganic materials | + Biocompatible materials with various shapes and sizes + Can be integrated into theranostic agents − Nanoparticle toxicity or off-site accumulation | MMP-responsive silica [339] and iron oxide nanoparticles [340] for targeted drug release |
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Vizovisek, M.; Ristanovic, D.; Menghini, S.; Christiansen, M.G.; Schuerle, S. The Tumor Proteolytic Landscape: A Challenging Frontier in Cancer Diagnosis and Therapy. Int. J. Mol. Sci. 2021, 22, 2514. https://doi.org/10.3390/ijms22052514
Vizovisek M, Ristanovic D, Menghini S, Christiansen MG, Schuerle S. The Tumor Proteolytic Landscape: A Challenging Frontier in Cancer Diagnosis and Therapy. International Journal of Molecular Sciences. 2021; 22(5):2514. https://doi.org/10.3390/ijms22052514
Chicago/Turabian StyleVizovisek, Matej, Dragana Ristanovic, Stefano Menghini, Michael G. Christiansen, and Simone Schuerle. 2021. "The Tumor Proteolytic Landscape: A Challenging Frontier in Cancer Diagnosis and Therapy" International Journal of Molecular Sciences 22, no. 5: 2514. https://doi.org/10.3390/ijms22052514