Myeloid-Derived Suppressor Cells: Major Figures that Shape the Immunosuppressive and Angiogenic Network in Cancer
Open accessAbstract
Myeloid-derived suppressor cells (MDSCs) constitute a vast population of immature myeloid cells implicated in various conditions. Most notably, their role in cancer is of great complexity. They exert immunosuppressive functions like hampering cancer immunity mediated by T lymphocytes and natural killer cells, while simultaneously they can recruit T regulatory cells to further promote immunosuppression, thus shielding tumor cells against the immune defenses. In addition, they were shown to support tumor invasion and metastasis by inducing vascularization. Yet again, in order to exert their angiogenic activities, they do have at their disposal a variety of occasionally overlapping mechanisms, mainly driven by VEGF/JAK/STAT signaling. In this concept, they have risen to be a rather attractive target for therapies, including depletion or maturation, so as to overcome cancer immunity and suppress angiogenic activity. Even though, many studies have been conducted to better understand these cells, there is much to be done yet. This article hopes to shed some light on the paradoxal complexity of these cells, while elucidating some of the key features of MDSCs in relation to immunosuppression and, most importantly, to the vascularization processes, along with current therapeutic options in cancer, in relation to MDSC depletion.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
HIF activation in hypoxia enhances immune suppressive effects of myeloid-derived suppressor cells.
“Furthermore, HIF activation in hypoxia enhances immune suppressive effects of myeloid-derived suppressor cells [50].”
From Hypoxia Signaling in Cancer: From Basics to Clinical Practice (2021) · cites this paper as [50]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Myeloid-derived-suppressor cells as regulators of the immune system
Gabrilovich, D. I., & Nagaraj, S. (2009) · Nature Reviews Immunology · doi:10.1038/nri2506 · Cited by 6,753 · see citing works
Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards
Bronte, V., Brandau, S., Chen, S.-H., Colombo, M. P., Frey, A. B., Greten, T. F., Mandruzzato, S., Murray, P. J., Ochoa, A., Ostrand-Rosenberg, S., et al. (2016) · Nature Communications · doi:10.1038/ncomms12150 · Cited by 2,751 · see citing works
Noman, M. Z., Desantis, G., Janji, B., Hasmim, M., Karray, S., Dessen, P., Bronte, V., & Chouaib, S. (2014) · Journal of Experimental Medicine · doi:10.1084/jem.20131916 · Cited by 2,166 · see citing works
The Nature of Myeloid-Derived Suppressor Cells in the Tumor Microenvironment
Kumar, V., Patel, S., Tcyganov, E., & Gabrilovich, D. I. (2016) · Trends in Immunology · doi:10.1016/j.it.2016.01.004 · Cited by 2,008 · see citing works
Myeloid-Derived Suppressor Cells
Gabrilovich, D. I. (2017) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-16-0297 · Cited by 1,890 · see citing works
Shibuya, M. (2011) · Genes & Cancer · doi:10.1177/1947601911423031 · Cited by 1,778 · see citing works
Myeloid-derived suppressor cells coming of age
Veglia, F., Perego, M., & Gabrilovich, D. I. (2018) · Nature Immunology · doi:10.1038/s41590-017-0022-x · Cited by 1,774 · see citing works
IL-17-producing γδ T cells and neutrophils conspire to promote breast cancer metastasis
Coffelt, S. B., Kersten, K., Doornebal, C. W., Weiden, J., Vrijland, K., Hau, C.-S., Verstegen, N. J. M., Ciampricotti, M., Hawinkels, L. J. A. C., Jonkers, J., et al. (2015) · Nature · doi:10.1038/nature14282 · Cited by 1,703 · see citing works
Žilionis, R., Engblom, C., Pfirschke, C., Savova, V., Zemmour, D., Saatcioglu, H. D., Krishnan, I., Maroni, G., Meyerovitz, C. V., Kerwin, C. M., et al. (2019) · Immunity · doi:10.1016/j.immuni.2019.03.009 · Cited by 1,483 · see citing works
History of myeloid-derived suppressor cells
Talmadge, J. E., & Gabrilovich, D. I. (2013) · Nature Reviews Cancer · doi:10.1038/nrc3581 · Cited by 1,148 · see citing works
An Immune Atlas of Clear Cell Renal Cell Carcinoma
Chevrier, S., Levine, J., Zanotelli, V. R., Siliņa, K., Schulz, D., Bacac, M., Ries, C. H., Ailles, L., Jewett, M. A. S., Moch, H., et al. (2017) · Cell · doi:10.1016/j.cell.2017.04.016 · Cited by 1,009 · see citing works
Ko, J. S., Zea, A. H., Rini, B. I., Ireland, J. L., Elson, P. J., Cohen, P. A., Golshayan, A., Rayman, P. A., Wood, L. S., García, J. A., et al. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-1332 · Cited by 861 · see citing works
Immunosuppression mediated by myeloid-derived suppressor cells (MDSCs) during tumour progression
Groth, C., Hu, X., Weber, R., Fleming, V., Altevogt, P., Utikal, J. S., & Umansky, V. (2018) · British Journal of Cancer · doi:10.1038/s41416-018-0333-1 · Cited by 846 · see citing works
Targeting VEGF/VEGFR to modulate antitumor immunity
Yang, J., Yan, J., & Liu, B. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00978 · Cited by 646 · see citing works
Role of tumor associated macrophages in tumor angiogenesis and lymphangiogenesis
Riabov, V., Gudima, A., Wang, N., Mickley, A., Orekhov, A. N., & Kzhyshkowska, J. G. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00075 · Cited by 631 · see citing works
The PD1:PD-L1/2 Pathway from Discovery to Clinical Implementation
Bardhan, K., Anagnostou, T., & Boussiotis, V. A. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00550 · Cited by 606 · see citing works
Ostrand-Rosenberg, S., Sinha, P., Beury, D. W., & Clements, V. K. (2012) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2012.01.011 · Cited by 583 · see citing works
Dolcetti, L., Peranzoni, E., Ugel, S., Marigo, I., Fernández, A., Mesa, C., Geilich, M., Winkels, G., Traggiai, E., Casati, A., et al. (2009) · European Journal of Immunology · doi:10.1002/eji.200939903 · Cited by 568 · see citing works
Myeloid-Derived Suppressor Cells Hinder the Anti-Cancer Activity of Immune Checkpoint Inhibitors
Weber, R., Fleming, V., Hu, X., Nagibin, V. S., Groth, C., Altevogt, P., Utikal, J. S., & Umansky, V. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01310 · Cited by 535 · see citing works
Ostrand-Rosenberg, S., & Fenselau, C. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1701019 · Cited by 509 · see citing works
Obermajer, N., Muthuswamy, R., Lesnock, J. L., Edwards, R. P., & Kaliński, P. (2011) · Blood · doi:10.1182/blood-2011-07-365825 · Cited by 499 · see citing works
Myeloid-Derived Suppressor Cells
Parker, K. H., Beury, D. W., & Ostrand‐Rosenberg, S. (2015) · Advances in cancer research · doi:10.1016/bs.acr.2015.04.002 · Cited by 482 · see citing works
LXR/ApoE Activation Restricts Innate Immune Suppression in Cancer
Tavazoie, M. F., Pollack, I., Tanqueco, R., Ostendorf, B. N., Reis, B. S., Gonsalves, F. C., Kurth, I., Andreu-Agullo, C., Derbyshire, M. L., Posada, J., et al. (2018) · Cell · doi:10.1016/j.cell.2017.12.026 · Cited by 476 · see citing works
An interleukin-17-mediated paracrine network promotes tumor resistance to anti-angiogenic therapy
Chung, A. S., Wu, X., Zhuang, G., Ngu, H., Kasman, I., Zhang, J., Vernes, J.-M., Jiang, Z., Meng, Y. G., Peale, F. V., et al. (2013) · Nature Medicine · doi:10.1038/nm.3291 · Cited by 445 · see citing works
The Role of Myeloid-Derived Suppressor Cells (MDSC) in Cancer Progression
Umansky, V., Blattner, C., Gebhardt, C., & Utikal, J. S. (2016) · Vaccines · doi:10.3390/vaccines4040036 · Cited by 440 · see citing works
Interleukin-8 in cancer pathogenesis, treatment and follow-up
Alfaro, C., Sanmamed, M. F., Rodriguez-Ruiz, M. E., Teijeira, Á., Oñate, C., González, Á., Ponz‐Sarvisé, M., Schalper, K. A., Perez‐Gracia, J. L., & Melero, I. (2017) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2017.08.004 · Cited by 373 · see citing works
Transcriptional regulation of myeloid-derived suppressor cells
Condamine, T., Mastio, J., & Gabrilovich, D. I. (2015) · Journal of Leukocyte Biology · doi:10.1189/jlb.4ri0515-204r · Cited by 372 · see citing works
Resistance to Anti-Angiogenic Therapy in Cancer—Alterations to Anti-VEGF Pathway
Itatani, Y., Kawada, K., Yamamoto, T. S., & Sakai, Y. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19041232 · Cited by 352 · see citing works
Reactive Oxygen Species as Regulators of MDSC-Mediated Immune Suppression
Ohl, K., & Tenbrock, K. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02499 · Cited by 335 · see citing works
He, D., Li, H., Yusuf, N., Elmets, C. A., Li, J., Mountz, J. D., & Xu, H. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0902574 · Cited by 334 · see citing works
Recent advances on anti-angiogenesis receptor tyrosine kinase inhibitors in cancer therapy
Qin, S., Li, A., Yi, M., Yu, S., Zhang, M., & Wu, K. (2019) · Journal of Hematology & Oncology · doi:10.1186/s13045-019-0718-5 · Cited by 328 · see citing works
Deryugina, E. I., Zając, E., Juncker‐Jensen, A., Kupriyanova, T. A., Welter, L. M., & Quigley, J. P. (2014) · Neoplasia · doi:10.1016/j.neo.2014.08.013 · Cited by 304 · see citing works
MDSCs: Key Criminals of Tumor Pre-metastatic Niche Formation
Wang, Y., Ding, Y., Guo, N., & Wang, S. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00172 · Cited by 282 · see citing works
Horikawa, N., Abiko, K., Matsumura, N., Hamanishi, J., Baba, T., Yamaguchi, K. D., Yoshioka, Y., Koshiyama, M., & Konishi, I. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-0387 · Cited by 276 · see citing works
IL-1 Family Cytokine Regulation of Vascular Permeability and Angiogenesis
Fahey, E., & Doyle, S. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01426 · Cited by 276 · see citing works
Zhang, B., Wang, Z., Wu, L., Zhang, M., Li, W., Ding, J., Zhu, J., Wei, H., & Zhao, K. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057114 · Cited by 273 · see citing works
Tumor-derived exosomes, myeloid-derived suppressor cells, and tumor microenvironment
Tian, X., Shen, H., Li, Z., Wang, T., & Wang, S. (2019) · Journal of Hematology & Oncology · doi:10.1186/s13045-019-0772-z · Cited by 261 · see citing works
Homeostatic and pathogenic extramedullary hematopoiesis
Kim, C. H. (2010) · Journal of Blood Medicine · doi:10.2147/jbm.s7224 · Cited by 253 · see citing works
Zhu, X., Mulcahy, L. A., Mohammed, R. A., Lee, A. H. S., Franks, H., Kilpatrick, L. E., Yılmazer, A., Paish, E. C., Ellis, I. O., Patel, P. M., et al. (2008) · Breast Cancer Research · doi:10.1186/bcr2195 · Cited by 250 · see citing works
Parker, K. H., Sinha, P., Horn, L. A., Clements, V. K., Yang, H., Li, J., Tracey, K. J., & Ostrand‐Rosenberg, S. (2014) · Cancer Research · doi:10.1158/0008-5472.can-13-2347 · Cited by 246 · see citing works
On the origin of myeloid-derived suppressor cells
Millrud, C. R., Bergenfelz, C., & Leandersson, K. (2016) · Oncotarget · doi:10.18632/oncotarget.12278 · Cited by 232 · see citing works
Phenotype, development, and biological function of myeloid-derived suppressor cells
Zhao, Y., Wu, T., Shao, S., Shi, B., & Zhao, Y. X. (2015) · OncoImmunology · doi:10.1080/2162402x.2015.1004983 · Cited by 220 · see citing works
Bruno, A., Mortara, L., Baci, D., Noonan, D. M., & Albini, A. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00771 · Cited by 216 · see citing works
Exosomes miR-126a released from MDSC induced by DOX treatment promotes lung metastasis
Deng, Z., Rong, Y., Teng, Y., Zhuang, X., Samykutty, A. K., Mu, J., Zhang, L., Cao, P., Yan, J., Miller, D. M., et al. (2016) · Oncogene · doi:10.1038/onc.2016.229 · Cited by 209 · see citing works
Human Tumor-Infiltrating Myeloid Cells: Phenotypic and Functional Diversity
Elliott, L., Doherty, G. A., Sheahan, K. D., & Ryan, E. J. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00086 · Cited by 208 · see citing works
Antonios, J. P., Soto, H., Everson, R. G., Moughon, D., Orpilla, J. R., Shin, N. P., Sedighim, S., Treger, J., Odesa, S., Tucker, A., et al. (2017) · Neuro-Oncology · doi:10.1093/neuonc/now287 · Cited by 206 · see citing works
Complexity and challenges in defining myeloid-derived suppressor cells
Damuzzo, V., Pinton, L., Desantis, G., Solito, S., Marigo, I., Bronte, V., & Mandruzzato, S. (2014) · Cytometry Part B Clinical Cytometry · doi:10.1002/cyto.b.21206 · Cited by 205 · see citing works
Mast Cells, Angiogenesis and Lymphangiogenesis in Human Gastric Cancer
Sammarco, G., Varricchi, G., Ferraro, V., Ammendola, M., Fazio, M. D., Altomare, D. F., Luposella, M., Maltese, L., Currò, G., Marone, G., et al. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092106 · Cited by 201 · see citing works
Mao, Y., Poschke, I. C., Wennerberg, E., de Coaña, Y. P., Brage, S. E., Schultz, I., Hansson, J., Masucci, G. V., Lundqvist, A., & Kiessling, R. W. (2013) · Cancer Research · doi:10.1158/0008-5472.can-12-4115 · Cited by 192 · see citing works
On the armament and appearances of human myeloid-derived suppressor cells
Poschke, I. C., & Kiessling, R. W. (2012) · Clinical Immunology · doi:10.1016/j.clim.2012.06.003 · Cited by 176 · see citing works
Zhu, C., Kros, J. M., Cheng, C., & Mustafa, D. A. M. (2017) · Neuro-Oncology · doi:10.1093/neuonc/nox081 · Cited by 176 · see citing works
Circulating and Tumor Myeloid-derived Suppressor Cells in Resectable Non–Small Cell Lung Cancer
Yamauchi, Y., Safi, S., Blattner, C., Rathinasamy, A., Umansky, L., Juenger, S., Warth, A., Eichhorn, M., Muley, T., Herth, F. J. F., et al. (2018) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201708-1707oc · Cited by 169 · see citing works
Intertwined regulation of angiogenesis and immunity by myeloid cells
Rivera, L. B., & Bergers, G. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.02.005 · Cited by 158 · see citing works
Exosomes from Myeloid-Derived Suppressor Cells Carry Biologically Active Proteins
Burke, M. C., Choksawangkarn, W., Edwards, N. J., Ostrand‐Rosenberg, S., & Fenselau, C. (2013) · Journal of Proteome Research · doi:10.1021/pr400879c · Cited by 157 · see citing works
Mi, Y., Guo, N., Luan, J., Cheng, J., Hu, Z., Jiang, P., Jin, W., & Gao, X. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00737 · Cited by 150 · see citing works
PGE2-Driven Induction and Maintenance of Cancer-Associated Myeloid-Derived Suppressor Cells
Obermajer, N., Wong, J. L., Edwards, R. P., Odunsi, K. O., Moysich, K. B., & Kaliński, P. (2012) · Immunological Investigations · doi:10.3109/08820139.2012.695417 · Cited by 144 · see citing works
Complexity and challenges in defining myeloid-derived suppressor cells
Damuzzo, V., Pinton, L., Desantis, G., Solito, S., Marigo, I., Bronte, V., & Mandruzzato, S. (2014) · Cytometry Part B Clinical Cytometry · doi:10.1002/cytob.21206 · Cited by 136 · see citing works
Activated T cells sustain myeloid-derived suppressor cell-mediated immune suppression
Pinton, L., Solito, S., Damuzzo, V., Francescato, S., Pozzuoli, A., Berizzi, A., D, S. M. M., Rossi, C. R., Bronte, V., & Mandruzzato, S. (2015) · Oncotarget · doi:10.18632/oncotarget.6662 · Cited by 124 · see citing works
STAT3 in Tumor-Associated Myeloid Cells: Multitasking to Disrupt Immunity
Su, Y., Banerjee, S., White, S. V., & Kortylewski, M. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19061803 · Cited by 123 · see citing works
Vetsika, E., Koinis, F., Gioulbasani, M., Aggouraki, D., Koutoulaki, A., Skalidaki, E., Mavroudis, D., Georgoulias, V., & Kotsakis, A. P. (2014) · Journal of Immunology Research · doi:10.1155/2014/659294 · Cited by 121 · see citing works
Self-citationBauer, R., Udonta, F., Wroblewski, M., Batalla, I. B., Santos, I. M., Taverna, F., Kuhlencord, M., Gensch, V., Päsler, S., Vinckier, S., et al. (2018) · Cancer Research · doi:10.1158/0008-5472.can-17-3415 · Cited by 114 · see citing works
Bozkus, C. C., Elzey, B. D., Crist, S. A., Ellies, L. G., & Ratliff, T. L. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1500959 · Cited by 112 · see citing works
Ma, P., Beatty, P. L., McKolanis, J., Brand, R. E., Schoen, R. E., & Finn, O. J. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01401 · Cited by 108 · see citing works
Geis-Asteggiante, L., Belew, A. T., Clements, V. K., Edwards, N. J., Ostrand-Rosenberg, S., El-Sayed, N. M., & Fenselau, C. (2018) · Journal of Proteome Research · doi:10.1021/acs.jproteome.7b00646 · Cited by 104 · see citing works
Koinis, F., Vetsika, E., Aggouraki, D., Skalidaki, E., Koutoulaki, A., Gkioulmpasani, M., Georgoulias, V., & Kotsakis, A. P. (2016) · Journal of Thoracic Oncology · doi:10.1016/j.jtho.2016.04.026 · Cited by 102 · see citing works
Self-citationShou, D., Wen, L., Song, Z., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.11352 · Cited by 101 · see citing works
Iwata, T., Kondo, Y., Kimura, O. S., Morosawa, T., Fujisaka, Y., Umetsu, T., Kogure, T., Inoue, J., Nakagome, Y., & Shimosegawa, T. (2016) · Scientific Reports · doi:10.1038/srep39296 · Cited by 100 · see citing works
Hsu, Y., Yen, M., Chang, W., Tsai, P.-H., Pan, Y., Liao, S., & Kuo, P. (2019) · Breast Cancer Research · doi:10.1186/s13058-019-1114-3 · Cited by 97 · see citing works
The Role of Exosomal MicroRNAs in the Tumor Microenvironment of Breast Cancer
Liu, Q., Peng, F., & Chen, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20163884 · Cited by 97 · see citing works
Binsfeld, M., Muller, J., Lamour, V., Veirman, K. D., Raeve, H. D., Bellahcène, A., Valckenborgh, E. V., Baron, F., Beguin, Y. P., Caers, J., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.9270 · Cited by 93 · see citing works
Lee, C., Lee, W., Cho, S. K., & Park, S. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19030869 · Cited by 93 · see citing works
Bosiljcic, M., Cederberg, R. A., Hamilton, M. J., LePard, N. E., Harbourne, B., Collier, J. L., Halvorsen, E. C., Shi, R., Franks, S. E., Kim, A. Y., et al. (2019) · Breast Cancer Research · doi:10.1186/s13058-019-1189-x · Cited by 89 · see citing works
Liu, J., Deng, W., Chen, L., Li, Y., Wu, L., Ma, S., Zhang, W., Bu, L., & Sun, Z. (2017) · Molecular Carcinogenesis · doi:10.1002/mc.22767 · Cited by 82 · see citing works
Tumour-infiltrating neutrophils counteract anti-VEGF therapy in metastatic colorectal cancer
Schiffmann, L. M., Fritsch, M., Gebauer, F., Günther, S. D., Stair, N., Seeger, J. M., Thangarajah, F., Dieplinger, G., Bludau, M., Alakus, H., et al. (2018) · British Journal of Cancer · doi:10.1038/s41416-018-0198-3 · Cited by 79 · see citing works
Combinatorial Approaches With Checkpoint Inhibitors to Enhance Anti-tumor Immunity
Seliger, B. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00999 · Cited by 77 · see citing works
Lu, L., Chang, C., & Hsu, C. (2019) · Journal of Hepatocellular Carcinoma · doi:10.2147/jhc.s159693 · Cited by 71 · see citing works
LncRNA HOTAIR in Tumor Microenvironment: What Role?
Botti, G., Scognamiglio, G., Aquino, G., Liguori, G., & Cantile, M. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092279 · Cited by 71 · see citing works
Piao, Y., Park, S. Y., Henry, V. K., Smith, B. D., Tiao, N., Flynn, D. L., & de Groot, J. (2016) · Neuro-Oncology · doi:10.1093/neuonc/now030 · Cited by 68 · see citing works
Mucha, J., Majchrzak, K., Taciak, B., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103249 · Cited by 65 · see citing works
Guédez, L., Jensen-Taubman, S., Bourboulia, D., Kwityn, C., Wei, B., Caterina, J. J., & Stetler‐Stevenson, W. G. (2012) · Journal of Immunotherapy · doi:10.1097/cji.0b013e3182619c8e · Cited by 63 · see citing works
Improving cancer immunotherapy by targeting the STATe of MDSCs
de Haas, N., de Koning, C. C. H., Spilgies, L. M., de Vries, I. J. M., & Hato, S. V. (2016) · OncoImmunology · doi:10.1080/2162402x.2016.1196312 · Cited by 63 · see citing works
Therapeutic Impact of Nanoparticle Therapy Targeting Tumor-Associated Macrophages
Penn, C. A., Yang, K., Zong, H., Lim, J. Y., Cole, A., Yang, D., Baker, J. R., Goonewardena, S. N., & Buckanovich, R. J. (2017) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-17-0688 · Cited by 63 · see citing works
Pro-Tumoral Inflammatory Myeloid Cells as Emerging Therapeutic Targets
Szebeni, G. J., Vízler, C., Nagy, L. I., Kitajka, K., & Puskás, L. G. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17111958 · Cited by 56 · see citing works
Identification of a G-CSF-Granulocytic MDSC axis that promotes tumor progression
Abrams, S. I., & Waight, J. D. (2012) · OncoImmunology · doi:10.4161/onci.19334 · Cited by 54 · see citing works
Shvedova, A. A., Kisin, E. R., Yanamala, N. V. K., Tkach, A. V., Gutkin, D. W., Star, A., Shurin, G. V., Kagan, V. E., & Shurin, M. R. (2015) · Cancer Research · doi:10.1158/0008-5472.can-14-2376 · Cited by 53 · see citing works
Notch Signaling in Myeloid Cells as a Regulator of Tumor Immune Responses
Hossain, F. M., Majumder, S., Uçar, D. A., Rodrı́guez, P. C., Golde, T. E., Minter, L. M., Osborne, B. A., & Miele, L. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01288 · Cited by 51 · see citing works
Targeting Myeloid Cells in Combination Treatments for Glioma and Other Tumors
Ding, A. S., Routkevitch, D., Jackson, C., & Lim, M. K. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01715 · Cited by 50 · see citing works
Zöller, M. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00137 · Cited by 47 · see citing works
Ibáñez-Vea, M., Zuazo, M., Gato, M., Arasanz, H., Fernández-Hinojal, G., Escors, D., & Kochan, G. T. (2017) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-017-0492-4 · Cited by 45 · see citing works
Chouaı̈b, S., Umansky, V., & Kiéda, C. (2018) · Współczesna Onkologia · doi:10.5114/wo.2018.73874 · Cited by 45 · see citing works
GUAN, X., Liu, Z., Zhang, J., & Jin, X. (2018) · Advances in Clinical and Experimental Medicine · doi:10.17219/acem/70065 · Cited by 34 · see citing works
Long Non-coding RNAs: Regulators of the Activity of Myeloid-Derived Suppressor Cells
Leija-Montoya, A. G., González-Ramírez, J., Sandoval-Basilio, J., Serafín-Higuera, I. R., Isiordia‐Espinoza, M. A., González‐González, R., & Serafín‐Higuera, N. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01734 · Cited by 26 · see citing works
Pilátová, K., Bencsiková, B., Demlová, R., Valík, D., & Dubská, L. Z. (2018) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-018-2166-4 · Cited by 21 · see citing works
C/EBP-δ positively regulates MDSC expansion and endothelial VEGFR2 expression in tumor development
Min, Y., Li, J., Qu, P., & Lin, P. C. (2017) · Oncotarget · doi:10.18632/oncotarget.16410 · Cited by 16 · see citing works
Delineating Pro-Angiogenic Myeloid Cells in Cancer Therapy
Johnson, B. W., Achyut, B. R., Fulzele, S., Mondal, A. K., Kolhe, R. B., & Arbab, A. S. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19092565 · Cited by 16 · see citing works
Pingwara, R., Witt-Jurkowska, K., Ulewicz, K., et al. (2017) · PubMed · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Phototherapy in cancer treatment: strategies and challenges
Cai, Y., Chai, T., Nguyen, W., Liu, J., Xiao, E., Ran, X., Ran, Y., Du, D., Chen, W., & Chen, X. (2025) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-025-02140-y · Cited by 453 · see citing works
Hack, S. P., Zhu, A. X., & Wang, Y. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.598877 · Cited by 286 · see citing works
Tumor hypoxia: From basic knowledge to therapeutic implications
Liao, C., Liu, X., Zhang, C., & Zhang, Q. (2023) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2022.12.011 · Cited by 223 · see citing works
Hypoxia Signaling in Cancer: From Basics to Clinical Practice
Sebestyén, A., Kopper, L., Dankó, T., & Tímár, J. (2021) · Pathology and Oncology Research · doi:10.3389/pore.2021.1609802 · Cited by 110 · see citing works
- Authors
- Vetsika, E.-K., Koukos, A., & Kotsakis, A.
- Affiliations
- National and Kapodistrian University of Athens (GR)
- University of Crete (GR)
- University of Thessaly (GR)
- Corresponding author
- Kotsakis, Athanasios
- Venue
- Cells
- Publisher
- MDPI AG
- Published
- 2019-12-15
- Volume
- 8
- Issue
- 12
- Pages
- 1647
- ISSN
- 2073-4409 (ISSN-L)
- PMC
- PMC6953061
- OpenAlex
- W2994769926
- Cited by
- 125
- References
- 96
- Citations by year
- 2026: 10 · 2025: 21 · 2024: 13 · 2023: 21 · 2022: 20 · 2021: 21 · 2020: 17 · 2019: 1 · 2018: 1
- FWCI
- 1.27
- Type
- journal article
- Language
- en
- Open access
- gold
- dx.doi.org
- Licence
- Locations
- Cells (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- University of Thessaly Institutional Repository (University of Thessaly) (submittedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- myeloid-derived suppressor cells, tumor immunosuppression, tumor angiogenesis, regulatory T cells, metastasis, tumor vascularization, cancer immunotherapy
- MeSH terms
- Myeloid-Derived Suppressor Cells, Humans, Immune Tolerance, Immunosuppression Therapy, Killer Cells, Natural, Neoplasms, T-Lymphocytes, Signal Transduction, Neovascularization, Physiologic, Myeloid Cells, Receptors, Vascular Endothelial Growth Factor, Histone Deacetylase Inhibitors, Tumor Microenvironment
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
