Thrombin contributes to cancer immune evasion via proteolysis of platelet-bound GARP to activate LTGF-β

Global cancer statistics, 2012

Torre, L. A., Bray, F., Siegel, R. L., Ferlay, J., Lortet‐Tieulent, J., & Jemal, A. (2015) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.21262 · Cited by 26,858

SWISS-MODEL: homology modelling of protein structures and complexes

Waterhouse, A. M., Bertoni, M., Bienert, S., Studer, G., Tauriello, G., Gumienny, R., Heer, F. T., de Beer, T., Rempfer, C., Bordoli, L., et al. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky427 · Cited by 13,248

FlowSOM: Using self‐organizing maps for visualization and interpretation of cytometry data

Gassen, S. V., Callebaut, B., van Helden, M. J. G., Lambrecht, B. N., Demeester, P. M. A., Dhaene, T., & Saeys, Y. (2015) · Cytometry Part A · doi:10.1002/cyto.a.22625 · Cited by 1,930

TGFβ drives immune evasion in genetically reconstituted colon cancer metastasis

Tauriello, D. V. F., Palomo-Ponce, S., Stork, D., Berenguer-Llergo, A., Badia-Ramentol, J., Iglesias, M., Sevillano, M., Ibiza, S., Cañellas, A., Hernando-Momblona, X., et al. (2018) · Nature · doi:10.1038/nature25492 · Cited by 1,851

Mechanisms of Foxp3+ T Regulatory Cell-Mediated Suppression

Shevach, E. M. (2009) · Immunity · doi:10.1016/j.immuni.2009.04.010 · Cited by 1,787

TGF-β directly targets cytotoxic T cell functions during tumor evasion of immune surveillance

Thomas, D. A., & Massagué, J. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.10.012 · Cited by 1,355

Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism.

Bhowmick, N., Ghiassi, M., Bakin, A. V., Aakre, M., Lundquist, C., Engel, M., Arteaga, C., & Moses, H. (2001) · Molecular Biology of the Cell · doi:10.1091/mbc.12.1.27 · Cited by 1,087

Latent TGF-β structure and activation

Shi, M., Zhu, J., Wang, R., Chen, X., Mi, L., Walz, T., & Springer, T. A. (2011) · Nature · doi:10.1038/nature10152 · Cited by 1,013

The roles of TGFβ in the tumour microenvironment

Pickup, M. W., Novitskiy, S. V., & Moses, H. L. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3603 · Cited by 936

Overview of the coagulation system

Palta, S., Saroa, R., & Palta, A. (2014) · Indian Journal of Anaesthesia · doi:10.4103/0019-5049.144643 · Cited by 903

Roles of TGFβ in metastasis

Padua, D. M., & Massagué, J. (2008) · Cell Research · doi:10.1038/cr.2008.316 · Cited by 828

Immune-mediated eradication of tumors through the blockade of transforming growth factor-β signaling in T cells

Gorelik, L., & Flavell, R. A. (2001) · Nature Medicine · doi:10.1038/nm1001-1118 · Cited by 770

How good is automated protein docking?

Kozakov, D., Beglov, D., Bohnuud, T., Mottarella, S. E., Xia, B., Hall, D. R., & Vajda, S. (2013) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.24403 · Cited by 748

Platelets and Thrombin Generation

Monroe, D. M., Hoffman, M., & Roberts, H. R. (2002) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/01.atv.0000031340.68494.34 · Cited by 682

TGFβ1 Inhibits the Formation of Benign Skin Tumors, but Enhances Progression to Invasive Spindle Carcinomas in Transgenic Mice

Cui, W., Fowlis, D. J., Bryson, S., Duffie, E., Ireland, H., Balmain, A., & Akhurst, R. J. (1996) · Cell · doi:10.1016/s0092-8674(00)80127-0 · Cited by 628

CyTOF workflow: Differential discovery in high-throughput high-dimensional cytometry datasets

Nowicka, M., Krieg, C., Crowell, H. L., Weber, L. M., Hartmann, F. J., Guglietta, S., Becher, B., Levesque, M. P., & Robinson, M. D. (2017) · F1000Research · doi:10.12688/f1000research.11622.3 · Cited by 495

Platelet-Derived Transforming Growth Factor-β Down-Regulates NKG2D Thereby Inhibiting Natural Killer Cell Antitumor Reactivity

Kopp, H., Placke, T., & Salih, H. R. (2009) · Cancer Research · doi:10.1158/0008-5472.can-09-2123 · Cited by 485

GARP (LRRC32) is essential for the surface expression of latent TGF-β on platelets and activated FOXP3 + regulatory T cells

Tran, D. Q., Andersson, J., Wang, R., Ramsey, H. E., Unutmaz, D., & Shevach, E. M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901944106 · Cited by 473

Latent Transforming Growth Factor-β (TGF-β) Binding Proteins: Orchestrators of TGF-β Availability

Rifkin, D. B. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.r400029200 · Cited by 422

Pf4-Cre transgenic mice allow the generation of lineage-restricted gene knockouts for studying megakaryocyte and platelet function in vivo

Tiedt, R., Schomber, T., Hao-Shen, H., & Skoda, R. C. (2006) · Blood · doi:10.1182/blood-2006-04-020362 · Cited by 417

Compensation of Signal Spillover in Suspension and Imaging Mass Cytometry

Chevrier, S., Crowell, H. L., Zanotelli, V. R., Engler, S., Robinson, M. D., & Bodenmiller, B. (2018) · Cell Systems · doi:10.1016/j.cels.2018.02.010 · Cited by 407

Thrombin generation, fibrin clot formation and hemostasis

Wolberg, A. S., & Campbell, R. A. (2008) · Transfusion and Apheresis Science · doi:10.1016/j.transci.2007.12.005 · Cited by 356

Targeting the TGFβ pathway with galunisertib, a TGFβRI small molecule inhibitor, promotes anti-tumor immunity leading to durable, complete responses, as monotherapy and in combination with checkpoint blockade

Holmgaard, R. B., Schaer, D. A., Li, Y., Castaneda, S. P., Murphy, M. Y., Xu, X., Inigo, I., Dobkin, J., Manro, J. R., Iversen, P. W., et al. (2018) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-018-0356-4 · Cited by 356

Platelets subvert T cell immunity against cancer via GARP-TGFβ axis

Rachidi, S., Metelli, A., Riesenberg, B., Wu, B. X., Nelson, M. H., Wallace, C., Paulos, C. M., Rubinstein, M. P., Garrett-Mayer, E. S., Hennig, M., et al. (2017) · Science Immunology · doi:10.1126/sciimmunol.aai7911 · Cited by 347

Deadly allies: the fatal interplay between platelets and metastasizing cancer cells

Erpenbeck, L., & Schön, M. P. (2010) · Blood · doi:10.1182/blood-2009-10-247296 · Cited by 346

Cancer-associated thrombosis: the when, how and why

Fernandes, C. J. C. D. S., Morinaga, L. T. K., Alves, J. L., Castro, M. A., Calderaro, D., Jardim, C., & Souza, R. (2019) · European Respiratory Review · doi:10.1183/16000617.0119-2018 · Cited by 327

Bifunctional immune checkpoint-targeted antibody-ligand traps that simultaneously disable TGFβ enhance the efficacy of cancer immunotherapy

Ravi, R., Noonan, K. A., Pham, V., Bedi, R., Zhavoronkov, A., Ozerov, I. V., Makarev, E., V. Artemov, A., Wysocki, P. T., Mehra, R., et al. (2018) · Nature Communications · doi:10.1038/s41467-017-02696-6 · Cited by 325

Endoplasmic reticulum chaperone gp96 is required for innate immunity but not cell viability

Randow, F., & Seed, B. (2001) · Nature Cell Biology · doi:10.1038/ncb1001-891 · Cited by 316

Transforming Growth Factor Beta Family: Insight into the Role of Growth Factors in Regulation of Fracture Healing Biology and Potential Clinical Applications

Poniatowski, Ł. A., Wojdasiewicz, P., Gasik, R., & Szukiewicz, D. (2015) · Mediators of Inflammation · doi:10.1155/2015/137823 · Cited by 304

Direct thrombin inhibitors

Lee, C. J., & Ansell, J. (2011) · British Journal of Clinical Pharmacology · doi:10.1111/j.1365-2125.2011.03916.x · Cited by 289

Molecular Events in the Processing of Recombinant Type 1 Pre-Pro-Transforming Growth Factor Beta to the Mature Polypeptide

Gentry, L. E., Lioubin, M. N., Purchio, A. F., & Marquardt, H. (1988) · Molecular and Cellular Biology · doi:10.1128/mcb.8.10.4162 · Cited by 284

diffcyt: Differential discovery in high-dimensional cytometry via high-resolution clustering

Weber, L. M., Nowicka, M., Soneson, C., & Robinson, M. D. (2019) · Communications Biology · doi:10.1038/s42003-019-0415-5 · Cited by 262

Novel diagnostic biomarkers for prostate cancer

Madu, C. O., & Lu, Y. (2010) · Journal of Cancer · doi:10.7150/jca.1.150 · Cited by 261

Membrane protein GARP is a receptor for latent TGF‐β on the surface of activated human Treg

Stockis, J., Colau, D., Coulie, P. G., & Lucas, S. (2009) · European Journal of Immunology · doi:10.1002/eji.200939684 · Cited by 252

Platelet‐Rich Plasma‐Derived Fibrin Clot Formation Stimulates Collagen Synthesis in Periodontal Ligament and Osteoblastic Cells In Vitro

Kawase, T., Okuda, K., Wolff, L. F., & Yoshie, H. (2003) · Journal of Periodontology · doi:10.1902/jop.2003.74.6.858 · Cited by 230

TGF-β in T Cell Biology: Implications for Cancer Immunotherapy

Dahmani, A., & Delisle, J. (2018) · Cancers · doi:10.3390/cancers10060194 · Cited by 222

Role of TGFβ in regulation of the tumor microenvironment and drug delivery (Review)

Papageorgis, P., & Stylianopoulos, T. (2015) · International Journal of Oncology · doi:10.3892/ijo.2015.2816 · Cited by 213

TREM-1 ligand expression on platelets enhances neutrophil activation

Haselmayer, P., Große‐Hovest, L., von Landenberg, P., Schild, H., & Radsak, M. P. (2007) · Blood · doi:10.1182/blood-2007-01-069195 · Cited by 211

GARP regulates the bioavailability and activation of TGFβ

Wang, R., Zhu, J., Dong, X., Shi, M., Lu, C., & Springer, T. A. (2012) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-12-1018 · Cited by 188

A novel bifunctional anti-PD-L1/TGF-β Trap fusion protein (M7824) efficiently reverts mesenchymalization of human lung cancer cells

David, J. M., Dominguez, C., McCampbell, K. K., Gulley, J. L., Schlom, J., & Palena, C. (2017) · OncoImmunology · doi:10.1080/2162402x.2017.1349589 · Cited by 180

Quantitative Proteome Analysis of Human Plasma following in Vivo Lipopolysaccharide Administration Using 16O/18O Labeling and the Accurate Mass and Time Tag Approach

Qian, W., Monroe, M. E., Liu, T., Jacobs, J., Anderson, G., Shen, Y., Moore, R., Anderson, D. J., Zhang, R., Calvano, S. E., et al. (2005) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m500045-mcp200 · Cited by 167

Structural basis of latent TGF-β1 presentation and activation by GARP on human regulatory T cells

Liénart, S., Merceron, R., Vanderaa, C., Lambert, F., Colau, D., Stockis, J., van der Woning, B., de Haard, H., Saunders, M. J., Coulie, P. G., et al. (2018) · Science · doi:10.1126/science.aau2909 · Cited by 160

Resolving the identity myth: Key markers of functional CD4+FoxP3+ regulatory T cells

Chen, X., & Oppenheim, J. J. (2011) · International Immunopharmacology · doi:10.1016/j.intimp.2011.05.018 · Cited by 138

High-dimensional single-cell analysis reveals the immune signature of narcolepsy

Hartmann, F. J., Bernard‐Valnet, R., Queriault, C., Mrdjen, D., Weber, L. M., Galli, E., Krieg, C., Robinson, M. D., Nguyen, X., Dauvilliers, Y. A., et al. (2016) · The Journal of Experimental Medicine · doi:10.1084/jem.20160897 · Cited by 124

Combined Inhibition of TGF-β Signaling and the PD-L1 Immune Checkpoint Is Differentially Effective in Tumor Models

Sow, H. S., Ren, J., Camps, M. G. M., OSSENDORP, F. A., & ten Dijke, P. (2019) · Cells · doi:10.3390/cells8040320 · Cited by 112

Surface Expression of TGFβ Docking Receptor GARP Promotes Oncogenesis and Immune Tolerance in Breast Cancer

Metelli, A., Wu, B. X., Fugle, C. W., Rachidi, S., Sun, S., Zhang, Y., Wu, J. D., Tomlinson, S., Howe, P. H., Yang, Y., et al. (2016) · Cancer Research · doi:10.1158/0008-5472.can-16-1456 · Cited by 111

Blocking immunosuppression by human Tregs in vivo with antibodies targeting integrin αVβ8

Stockis, J., Liénart, S., Colau, D., Collignon, A., Nishimura, S. L., Sheppard, D., Coulie, P. G., & Lucas, S. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1710680114 · Cited by 111

The Molecular Chaperone gp96/GRP94 Interacts with Toll-like Receptors and Integrins via Its C-terminal Hydrophobic Domain

Wu, S., Hong, F., Gewirth, D. T., Guo, B., Liu, B., & Li, Z. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.309526 · Cited by 95

GP96 is a GARP chaperone and controls regulatory T cell functions

Zhang, Y., Wu, B. X., Metelli, A., Thaxton, J. E., Hong, F., Rachidi, S., Ansa-Addo, E., Sun, S., Vasu, C., Yang, Y., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci79014 · Cited by 95

Regulation of the Expression of GARP/Latent TGF-β1 Complexes on Mouse T Cells and Their Role in Regulatory T Cell and Th17 Differentiation

Edwards, J. P., Fujii, H., Zhou, A. X., Creemers, J. W. M., Unutmaz, D., & Shevach, E. M. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1300199 · Cited by 94

Blockade of only TGF-β 1 and 2 is sufficient to enhance the efficacy of vaccine and PD-1 checkpoint blockade immunotherapy

Terabe, M., Robertson, F. C., Clark, K. T., Ravin, E. D., Bloom, A. C., Venzon, D. J., Kato, S., Mirza, A. M., & Berzofsky, J. A. (2017) · OncoImmunology · doi:10.1080/2162402x.2017.1308616 · Cited by 89

Protection from tumor necrosis factor-mediated cytolysis by platelets.

Philippe, C., Philippe, B., Fouqueray, B. L., Perez, J., Lebret, M., & Baud, L. (1993) · PubMed Central · Cited by 83

Use of dabigatran etexilate to reduce breast cancer progression

DeFeo, K., Hayes, C. S., Chernick, M. R., van Ryn, J., & Gilmour, S. K. (2010) · Cancer Biology & Therapy · doi:10.4161/cbt.10.10.13236 · Cited by 73

GARP Dampens Cancer Immunity by Sustaining Function and Accumulation of Regulatory T Cells in the Colon

Salem, M., Wallace, C. H., Velegraki, M., Li, A., Ansa-Addo, E. A., Metelli, A., Kwon, H., Riesenberg, B., Wu, B. X., Zhang, Y., et al. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-2623 · Cited by 69

Cutting Edge: Active TGF-β1 Released from GARP/TGF-β1 Complexes on the Surface of Stimulated Human B Lymphocytes Increases Class-Switch Recombination and Production of IgA

Dedobbeleer, O., Stockis, J., van der Woning, B., Coulie, P. G., & Lucas, S. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1601882 · Cited by 64

Platelet count as a predictor of metastasis and venous thromboembolism in patients with cancer

Sylman, J. L., Mitrugno, A., Tormoen, G. W., Wagner, T. H., Mallick, P., & McCarty, O. J. T. (2017) · Convergent Science Physical Oncology · doi:10.1088/2057-1739/aa6c05 · Cited by 54

B lymphocytes confer immune tolerance via cell surface GARP-TGF-β complex

Wallace, C. H., Wu, B. X., Salem, M. A., Ansa-Addo, E. A., Metelli, A., Sun, S., Gilkeson, G. S., Shlomchik, M. J., Liu, B., & Li, Z. (2018) · JCI Insight · doi:10.1172/jci.insight.99863 · Cited by 50

Thrombin inhibition and cyclophosphamide synergistically block tumor progression and metastasis

Alexander, E. T., Minton, A. R., Hayes, C. S., Goss, A., van Ryn, J., & Gilmour, S. K. (2015) · Cancer Biology & Therapy · doi:10.1080/15384047.2015.1078025 · Cited by 42

GARP Is Regulated by miRNAs and Controls Latent TGF-β1 Production by Human Regulatory T Cells

Gauthy, E., Cuende, J., Stockis, J., Huygens, C., Lethé, B., Collet, J., Bommer, G. T., Coulie, P. G., & Lucas, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076186 · Cited by 41

Activated coagulation factors in human malignant effusions and their contribution to cancer cell metastasis and therapy

Lühr, I., Kunze, T., Mundhenke, C., Maass, N., Erhart, T., Denker, M., Beckmann, D., Tiemann, M., Schulte, C., Dohrmann, P., et al. (2007) · Thrombosis and Haemostasis · doi:10.1160/th06-12-0712 · Cited by 36

Dabigatran reduces thrombin-induced platelet aggregation and activation in a dose-dependent manner

Vinholt, P. J., Nielsen, C., Söderström, A., Brandes, A., & Nybo, M. (2017) · Journal of Thrombosis and Thrombolysis · doi:10.1007/s11239-017-1512-2 · Cited by 34

The effect of dabigatran and rivaroxaban on platelet reactivity and inflammatory markers

Zemer‐Wassercug, N., Haim, M., Leshem‐Lev, D., Orvin, K., Vaduganathan, M., Gutstein, A., Kadmon, E., Mager, A., Kornowski, R., & Lev, E. (2015) · Journal of Thrombosis and Thrombolysis · doi:10.1007/s11239-015-1245-z · Cited by 32

High platelet counts increase metastatic risk in huge hepatocellular carcinoma undergoing transarterial chemoembolization

Xue, T., Ge, N., Xu, X. Y., Le, F., Zhang, B., & Wang, Y. (2016) · Hepatology Research · doi:10.1111/hepr.12651 · Cited by 31

Dabigatran Potentiates Gemcitabine-Induced Growth Inhibition of Pancreatic Cancer in Mice

Shi, K., Damhofer, H., Daalhuisen, J. B., ten Brink, M. S., Richel, D. J., & Spek, C. A. (2017) · Molecular Medicine · doi:10.2119/molmed.2016.00214 · Cited by 24

The Role of Proteomics in Biomarker Development for Improved Patient Diagnosis and Clinical Decision Making in Prostate Cancer

Tonry, C. L., Leacy, E. J., Raso, C., Finn, S. P., Armstrong, J., & Pennington, S. R. (2016) · Diagnostics · doi:10.3390/diagnostics6030027 · Cited by 23

Targeting immunosuppression by Tregs with monoclonal antibodies against GARP

Liénart, S., Stockis, J., Dedobbeleer, O., & Lucas, S. (2016) · OncoImmunology · doi:10.1080/2162402x.2015.1074379 · Cited by 7

Perioperative changes in TGF-β1 levels predict the oncological outcome of cryoablation-receiving patients with localized prostate cancer

Wang, A. S.-S., Chen, C., Chou, Y., & Pu, Y. (2016) · Cryobiology · doi:10.1016/j.cryobiol.2016.05.011 · Cited by 6

TGFβ biology in cancer progression and immunotherapy

Derynck, R., Turley, S. J., & Akhurst, R. J. (2021) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-020-0403-1 · Cited by 944

Combination strategies to maximize the benefits of cancer immunotherapy

Zhu, S., Zhang, T., Zheng, L., Liu, H., Song, W., Liu, D., Li, Z., & Pan, C.-X. (2021) · Journal of Hematology & Oncology · doi:10.1186/s13045-021-01164-5 · Cited by 654

Overcoming TGFβ-mediated immune evasion in cancer

Tauriello, D. V. F., Sancho, E., & Batlle, E. (2022) · Nature Reviews Cancer · doi:10.1038/s41568-021-00413-6 · Cited by 377

TGF ‐β as a driver of fibrosis: physiological roles and therapeutic opportunities

Budi, E. H., Schaub, J. R., Decaris, M. L., Turner, S., & Derynck, R. (2021) · The Journal of Pathology · doi:10.1002/path.5680 · Cited by 310

TGF-β Regulation of T Cells

Chen, W. (2023) · Annual Review of Immunology · doi:10.1146/annurev-immunol-101921-045939 · Cited by 299

Thrombin contributes to cancer immune evasion via proteolysis of platelet-bound GARP for LTGF-β activation

Metelli, A., & Li, Z. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.204.supp.242.12

GARP-TGFβ Axis on Activated Platelets Supports Tumor Progression

Metelli, A., Wu, B. X., Riesenberg, B., Fugle, C. W., Sun, S., Liu, B., & Li, Z. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.198.supp.126.17

Platelets subvert T cell immunity against cancer via GARP-TGFβ axis

Rachidi, S., Metelli, A., Riesenberg, B., Wu, B. X., Nelson, M. H., Wallace, C., Paulos, C. M., Rubinstein, M. P., Garrett-Mayer, E. S., Hennig, M., et al. (2017) · Science Immunology · doi:10.1126/sciimmunol.aai7911 · Cited by 347

Immunomodulatory role of thrombin in cancer progression

Alexander, E. T., & Gilmour, S. K. (2022) · Molecular Carcinogenesis · doi:10.1002/mc.23398 · Cited by 32

Immunoregulatory functions and the therapeutic implications of GARP-TGF-β in inflammation and cancer

Metelli, A., Salem, M. A., Wallace, C. H., Wu, B. X., Li, A., Li, X., & Li, Z. (2018) · Journal of Hematology & Oncology · doi:10.1186/s13045-018-0570-z · Cited by 120