Cited by 332Immune cells in cancerPhagocytosis and Immune RegulationCancer, Stress, Anesthesia, and Immune Response

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The Role of Macrophages in Cancer Development and Therapy

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Cendrowicz, Ewa, Sas, Zuzanna, Bremer, Edwin, Rygiel, Tomasz P.·2021·Cancers

DOI 10.3390/cancers13081946PMC PMC8073377

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Abstract

Macrophages are critical mediators of tissue homeostasis and influence various aspects of immunity. Tumor-associated macrophages are one of the main cellular components of the tumor microenvironment. Depending on their activation status, macrophages can exert a dual influence on tumorigenesis by either antagonizing the cytotoxic activity of immune cells or, less frequently, by enhancing antitumor responses. In most situations, TAMs suppress T cell recruitment and function or regulate other aspects of tumor immunity. The importance of TAMs targeting in cancer therapy is derived from the strong association between the high infiltration of TAMs in the tumor tissue with poor patient prognosis. Several macrophage-targeting approaches in anticancer therapy are developed, including TAM depletion, inhibition of new TAM differentiation, or re-education of TAM activation for cancer cell phagocytosis. In this review, we will describe the role of TAMs in tumor development, including such aspects as protumorigenic inflammation, immune suppression, neoangiogenesis, and enhancement of tissue invasion and distant metastasis. Furthermore, we will discuss therapeutic approaches that aim to deplete TAMs or, on the contrary, re-educate TAMs for cancer cell phagocytosis and antitumor immunity.

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Figure 1 A spectrum of macrophage activation. The functional M1-M2 spectrum subdivisions of activated macrophages, derived from human monocytes or mouse bone marrow upon CSF-1 stimulation. Stimulation conditions are IL-4, immune complexes (Ic), IL-10, glucocorticoids (GC) with TGFβ, glucocorticoids alone, LPS, LPS and IFNγ, and IFNγ alone.CC BY · PubMed Central

Figure 2 Mechanisms of tumorigenesis stimulation by TAMs. TAMs play an important role in the process of tumorigenesis by induction of inflammation (top left loop), stimulation of neoangiogenesis (top right loop), immune suppression (bottom left loop), and induction of metastasis (bottom right loop). The figure was created with Biorender.com.CC BY · PubMed Central

Figure 3 Strategies to target TAMs for anticancer therapy. Two main strategies are used to target TAMs in the TME, reduction of the number of macrophages in the tumor (top panel) or re-education of macrophages (bottom panel). Several molecular targets have been discovered to apply therapies targeting TAMs (mentioned in the figure), and various therapeutics have been developed that target these molecules, including small molecule inhibitors, monoclonal antibodies, soluble ligands, bispecific fusion proteins, and antibody fragments, and nanoparticles. The figure was created with Biorender.com.CC BY · PubMed Central

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Recent Advances Targeting CCR5 for Cancer and Its Role in Immuno-Oncology
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Inhibition of colony stimulating factor-1 receptor abrogates microenvironment-mediated therapeutic resistance in gliomas
Yan, D., Kowal, J., Akkari, L., Schuhmacher, A. J., Huse, J. T., West, B. L., & Joyce, J. A. (2017) · Oncogene · doi:10.1038/onc.2017.261 · Cited by 238
Carlumab, an anti-C-C chemokine ligand 2 monoclonal antibody, in combination with four chemotherapy regimens for the treatment of patients with solid tumors: an open-label, multicenter phase 1b study
Braña, I., Calles, A., LoRusso, P. M., Yee, L., Puchalski, T. A., Seetharam, S., Zhong, B., de Boer, C. J., Tabernero, J. M., & Calvo, E. (2014) · Targeted Oncology · doi:10.1007/s11523-014-0320-2 · Cited by 233
The TLR7/8 agonist R848 remodels tumor and host responses to promote survival in pancreatic cancer
Michaelis, K. A., Norgard, M. A., Zhu, X., Levasseur, P. R., Sivagnanam, S., Liudahl, S. M., Burfeind, K. G., Olson, B. G., Pelz, K. R., Ramos, D. M. A., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12657-w · Cited by 231
The Crosstalk Between Tumor-Associated Macrophages (TAMs) and Tumor Cells and the Corresponding Targeted Therapy
Ge, Z., & Ding, S. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.590941 · Cited by 231
Targeting MARCO and IL37R on Immunosuppressive Macrophages in Lung Cancer Blocks Regulatory T Cells and Supports Cytotoxic Lymphocyte Function
Fleur, L. L., Botling, J., He, F., Pelicano, C., Zhou, C., He, C., Palano, G., Mezheyeuski, A., Micke, P., Ravetch, J. V., et al. (2020) · Cancer Research · doi:10.1158/0008-5472.can-20-1885 · Cited by 228
Topical resiquimod can induce disease regression and enhance T-cell effector functions in cutaneous T-cell lymphoma
Rook, A. H., Gelfand, J. M., Wysocka, M., Troxel, A. B., Benoit, B. M., Surber, C., Elenitsas, R., Buchanan, M., Leahy, D. S., Watanabe, R., et al. (2015) · Blood · doi:10.1182/blood-2015-02-630335 · Cited by 223
Phase I study of emactuzumab single agent or in combination with paclitaxel in patients with advanced/metastatic solid tumors reveals depletion of immunosuppressive M2-like macrophages
Gomez-Roca, C., Italiano, A., Tourneau, C. L., Cassier, P. A., Toulmonde, M., D’Angelo, S. P., Campone, M., WEBER, K. L., Loirat, D., Cannarile, M. A., et al. (2019) · Annals of Oncology · doi:10.1093/annonc/mdz163 · Cited by 223
Trabectedin, a drug acting on both cancer cells and the tumour microenvironment
D’Incalci, M., Badri, N., Galmarini, C. M., & Allavena, P. (2014) · British Journal of Cancer · doi:10.1038/bjc.2014.149 · Cited by 219
Phase I Study of the CD47 Blocker TTI-621 in Patients with Relapsed or Refractory Hematologic Malignancies
Ansell, S. M., Maris, M. B., Lesokhin, A. M., Chen, R. W., Flinn, I. W., Sawas, A., Minden, M. D., Villa, D. R., Percival, M. M., Advani, A. S., et al. (2021) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-20-3706 · Cited by 211
First-in-Human Study of AMG 820, a Monoclonal Anti-Colony-Stimulating Factor 1 Receptor Antibody, in Patients with Advanced Solid Tumors
Papadopoulos, K. P., Gluck, L., Martin, L. P., Olszanski, A. J., Tolcher, A. W., Ngarmchamnanrith, G., Rasmussen, E., Amore, B. M., Nagorsen, D., Hill, J. S., et al. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-3261 · Cited by 209
CAR T cell therapy: A new era for cancer treatment (Review)
Mohanty, R., Chowdhury, C. R., Arega, S., Sen, P., Ganguly, P., & Ganguly, N. (2019) · Oncology Reports · doi:10.3892/or.2019.7335 · Cited by 203
Phase 1b study of a small molecule antagonist of human chemokine (C-C motif) receptor 2 (PF-04136309) in combination with nab-paclitaxel/gemcitabine in first-line treatment of metastatic pancreatic ductal adenocarcinoma
Noel, M., O’Reilly, E. M., Wolpin, B. M., Ryan, D. P., Bullock, A. J., Britten, C. D., Linehan, D. C., Belt, B. A., Gamelin, E. C., Ganguly, B., et al. (2020) · Investigational New Drugs · doi:10.1007/s10637-019-00830-3 · Cited by 199
Targeting Macrophage-Recruiting Chemokines as a Novel Therapeutic Strategy to Prevent the Progression of Solid Tumors
Argyle, D. J., & Kitamura, T. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02629 · Cited by 195
Function of CSF1 and IL34 in Macrophage Homeostasis, Inflammation, and Cancer
Lin, W., Xu, D., Austin, C. D., Caplazi, P., Senger, K., Sun, Y., Jeet, S., Young, J., Delarosa, D., Suto, E., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02019 · Cited by 192
MerTK inhibition in tumor leukocytes decreases tumor growth and metastasis
Cook, R. S., Jacobsen, K. M., Wofford, A., DeRyckere, D., Stanford, J. C., Prieto, A. L., Redente, E. F., Sandahl, M. A., Hunter, D. M., Strunk, K. E., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci67655 · Cited by 191
Inhibition of the CCL2 receptor, CCR2, enhances tumor response to immune checkpoint therapy
Tu, M. M., Abdel-Hafiz, H. A., Jones, R. T., Jean, A., Hoff, K. J., Duex, J. E., Chauca-Diaz, A., Costello, J. C., Dancik, G. M., Tamburini, B. A. J., et al. (2020) · Communications Biology · doi:10.1038/s42003-020-01441-y · Cited by 185
Combined Effects of Pericytes in the Tumor Microenvironment
Ribeiro, A. L., & Okamoto, O. K. (2015) · Stem Cells International · doi:10.1155/2015/868475 · Cited by 173
Multiple myeloma cells recruit tumor-supportive macrophages through the CXCR4/CXCL12 axis and promote their polarization toward the M2 phenotype
Beider, K., Bitner, H., Leiba, M., Gutwein, O., Koren‐Michowitz, M., Ostrovsky, O., Abraham, M., Wald, H., Galun, E., Peled, A., et al. (2014) · Oncotarget · doi:10.18632/oncotarget.2207 · Cited by 171
TLR-3 Stimulation Skews M2 Macrophages to M1 Through IFN-αβ Signaling and Restricts Tumor Progression
Vidyarthi, A., Khan, N., Agnihotri, T., Negi, S., Das, D. K., Aqdas, M., Chatterjee, D., Colegio, O. R., Tewari, M. K., & Agrewala, J. N. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01650 · Cited by 163
Role of CD47 in Hematological Malignancies
Eladl, E., Tremblay‐LeMay, R., Rastgoo, N., Musani, R., Chen, W.-M., Liu, A., & Chang, H. (2020) · Journal of Hematology & Oncology · doi:10.1186/s13045-020-00930-1 · Cited by 163
Immune suppression and reversal of the suppressive tumor microenvironment
Shimizu, K., Iyoda, T., Okada, M., Yamasaki, S., & Fujii, S. (2018) · International Immunology · doi:10.1093/intimm/dxy042 · Cited by 162
The twin cytokines interleukin-34 and CSF-1: masterful conductors of macrophage homeostasis
Muñoz-García, J., Cochonneau, D., Télétchéa, S., Moranton, E., Lanoé, D., Brion, R., Lézot, F., Heymann, M., & Heymann, D. (2020) · Theranostics · doi:10.7150/thno.50683 · Cited by 161
High-Infiltration of Tumor-Associated Macrophages Predicts Unfavorable Clinical Outcome for Node-Negative Breast Cancer
Zhang, Y., Cheng, S., Zhang, M., Zhen, L., Pang, D., Zhang, Q., & Li, Z. (2013) · PLoS ONE · doi:10.1371/journal.pone.0076147 · Cited by 144
An ovarian tumor marker with homology to vaccinia virus contains an IgV-like region and multiple transmembrane domains.
Campbell, I., Freemont, P. S., Foulkes, W. D., & Trowsdale, J. (1992) · PubMed · Cited by 140
Prognostic Significance of Tumor-Associated Macrophage Content in Head and Neck Squamous Cell Carcinoma: A Meta-Analysis
Kumar, A., Knops, A. M., Swendseid, B. P., Martinez-Outschoom, U., Harshyne, L. A., Philp, N. J., Rodeck, U., Luginbuhl, A., Cognetti, D. M., Johnson, J. M., et al. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00656 · Cited by 140
CCL20 and CXCL8 synergize to promote progression and poor survival outcome in patients with colorectal cancer by collaborative induction of the epithelial–mesenchymal transition
Cheng, X., Li, Y., Tan, J. Y., Sun, B., Xiao, Y., Fang, X.-B., Zhang, X., Li, Q., Dong, J., Li, M., et al. (2014) · Cancer Letters · doi:10.1016/j.canlet.2014.03.008 · Cited by 138
F-box protein FBXW7 inhibits cancer metastasis in a non-cell-autonomous manner
Yumimoto, K., Akiyoshi, S., Ueo, H., Sagara, Y., Onoyama, I., Ueo, H., Ohno, S., Mori, M., Mimori, K., & Nakayama, K. I. (2015) · Journal of Clinical Investigation · doi:10.1172/jci78782 · Cited by 137
Peptide-guided resiquimod-loaded lignin nanoparticles convert tumor-associated macrophages from M2 to M1 phenotype for enhanced chemotherapy
Figueiredo, P., Lepland, A., Scodeller, P., Fontana, F., Torrieri, G., Tiboni, M., Shahbazi, M., Casettari, L., Kostiainen, M. A., Hirvonen, J. J., et al. (2020) · Acta Biomaterialia · doi:10.1016/j.actbio.2020.09.038 · Cited by 137
Tumor-associated macrophages modulate resistance to oxaliplatin via inducing autophagy in hepatocellular carcinoma
Fu, X.-T., Song, K., Zhou, J., Shi, Y.-H., Liu, W.-R., Shi, G., Gao, Q., Wang, X.-Y., Ding, Z.-B., & Fan, J. (2019) · Cancer Cell International · doi:10.1186/s12935-019-0771-8 · Cited by 133
CD40 Ligation Activates Murine Macrophages via an IFN-γ-Dependent Mechanism Resulting in Tumor Cell Destruction In Vitro
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Safety and efficacy of AMG 820, an anti-colony-stimulating factor 1 receptor antibody, in combination with pembrolizumab in adults with advanced solid tumors
Razak, A. R., Cleary, J. M., Moreno, V., Boyer, M. J., Calvo, E., Edenfield, W. J., Tie, J., Harvey, R. D., Rutten, A., Shah, M. A., et al. (2020) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2020-001006 · Cited by 124
Overview of CD24 as a new molecular marker in ovarian cancer
Tarhriz, V., Bandehpour, M., Dastmalchi, S., Ouladsahebmadarek, E., Zarredar, H., & Eyvazi, S. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27581 · Cited by 123
Tumor‑infiltrating M2�macrophages driven by specific genomic alterations are associated with prognosis in bladder cancer
Xue, Y., Tong, L., Liu, F., Liu, A., Zeng, S., Xiong, Q., Yang, Z., He, X., Sun, Y., & Xu, C. (2019) · Oncology Reports · doi:10.3892/or.2019.7196 · Cited by 122
Macrophages‐Triggered Sequential Remodeling of Endothelium‐Interstitial Matrix to Form Pre‐Metastatic Niche in Microfluidic Tumor Microenvironment
Kim, H., Chung, H., Kim, J., Choi, D., Shin, Y., Kang, Y. G., Kim, B., Seo, S., Chung, S. H., & Seok, S. H. (2019) · Advanced Science · doi:10.1002/advs.201900195 · Cited by 119
Synergy between Coproduced CC and CXC Chemokines in Monocyte Chemotaxis through Receptor-Mediated Events
Gouwy, M., Struyf, S., Noppen, S., Schutyser, E., Springael, J., Parmentier, M., Proost, P., & Damme, J. V. (2008) · Molecular Pharmacology · doi:10.1124/mol.108.045146 · Cited by 115
Macrophage checkpoint blockade: results from initial clinical trials, binding analyses, and CD47-SIRPα structure–function
Jalil, A. R., Andrechak, J. C., & Discher, D. E. (2020) · Antibody Therapeutics · doi:10.1093/abt/tbaa006 · Cited by 115
Interaction of CTLA‐4 (CD152) with CD80 or CD86 inhibits human T‐cell activation
Vandenborre, K., Gool, S. W. V., Kasran, A., Ceuppens, J. L., Boogaerts, M. A., & Vandenberghe, P. (1999) · Immunology · doi:10.1046/j.1365-2567.1999.00888.x · Cited by 113
Enhancing antibody-dependent cellular phagocytosis by Re-education of tumor-associated macrophages with resiquimod-encapsulated liposomes
Li, H., Somiya, M., & Kuroda, S. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2020.120601 · Cited by 107
Zoledronic acid impairs myeloid differentiation to tumour-associated macrophages in mesothelioma
Veltman, J. D., Lambers, M. E. H., van Nimwegen, M., Hendriks, R. W., Hoogsteden, H. C., Hegmans, J. P., & Aerts, J. G. J. V. (2010) · British Journal of Cancer · doi:10.1038/sj.bjc.6605814 · Cited by 104
Targeting PDGF‐mediated recruitment of pericytes blocks vascular mimicry and tumor growth
Thijssen, V. L., Paulis, Y. W. J., Nowak-Sliwinska, P. M., Deumelandt, K., Hosaka, K., Soetekouw, P. M. M. B., Cîmpean, A. M., Raica, M., Pauwels, P., van den Oord, J. J., et al. (2018) · The Journal of Pathology · doi:10.1002/path.5152 · Cited by 103
Promotion of tumor-associated macrophages infiltration by elevated neddylation pathway via NF-κB-CCL2 signaling in lung cancer
Zhou, L., Jiang, Y., Liu, X., Li, L., Yang, X., Dong, C., Liu, X., Lin, Y., Yan, L., Yu, J., et al. (2019) · Oncogene · doi:10.1038/s41388-019-0840-4 · Cited by 102
The activation status of human macrophages presenting antigen determines the efficiency of Th17 responses
Arnold, C. E., Gordon, P. M., Barker, R. N., & Wilson, H. M. (2014) · Immunobiology · doi:10.1016/j.imbio.2014.09.022 · Cited by 98
RRx-001 Acts as a Dual Small Molecule Checkpoint Inhibitor by Downregulating CD47 on Cancer Cells and SIRP-α on Monocytes/Macrophages
Cabrales, P. (2019) · Translational Oncology · doi:10.1016/j.tranon.2018.12.001 · Cited by 97
Resiquimod as an Immunologic Adjuvant for NY-ESO-1 Protein Vaccination in Patients with High-Risk Melanoma
Sabado, R. L., Pavlick, A. C., Gnjatic, S., Cruz, C. M., Vengco, I., Hasan, F., Spadaccia, M. R., Darvishian, F., Chiriboga, L. A., Holman, R. M., et al. (2015) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-14-0202 · Cited by 96
Overall survival in a trial of orally administered CCR2 inhibitor CCX872 in locally advanced/metastatic pancreatic cancer: Correlation with blood monocyte counts.
Linehan, D. C., Noel, M. S., Hezel, A. F., Wang‐Gillam, A., Eskens, F. A. L. M., Sleijfer, S., Desar, I. M. E., Erdkamp, F., Wilmink, J. W., Diehl, J., et al. (2018) · Journal of Clinical Oncology · doi:10.1200/jco.2018.36.5_suppl.92 · Cited by 93
Expression of scavenger receptor MARCO defines a targetable tumor‐associated macrophage subset in non‐small cell lung cancer
Fleur, L. L., Boura, V. F., Alexeyenko, A., Berglund, A., Pontén, V., Mattsson, J. S. M., Djureinovic, D., Persson, J., Brunnström, H., Isaksson, J., et al. (2018) · International Journal of Cancer · doi:10.1002/ijc.31545 · Cited by 93
FDA Approval Summary: Trabectedin for Unresectable or Metastatic Liposarcoma or Leiomyosarcoma Following an Anthracycline-Containing Regimen
Barone, A. K., Chi, D.-C., Theoret, M. R., Chen, H., He, K., Kufrin, D., Helms, W. S., Subramaniam, S., Zhao, H., Patel, A., et al. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-0898 · Cited by 89
Genetically engineered macrophages persist in solid tumors and locally deliver therapeutic proteins to activate immune responses
Brempelis, K. J., Cowan, C. M., Kreuser, S. A., Labadie, K. P., Prieskorn, B. M., Lieberman, N. A. P., Ene, C., Moyes, K. W., Chinn, H. K., DeGolier, K., et al. (2020) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2020-001356 · Cited by 84
Macrophages and tumor angiogenesis
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Prognostic significance of tumor-associated macrophages: past, present and future
Cortese, N., Carriero, R., Laghi, L., Mantovani, A., & Marchesi, F. (2020) · Seminars in Immunology · doi:10.1016/j.smim.2020.101408 · Cited by 83
Functional TRAIL receptors in monocytes and tumor-associated macrophages: A possible targeting pathway in the tumor microenvironment
Liguori, M., Buracchi, C., Pasqualini, F., Bergomas, F., Pesce, S., Sironi, M., Grizzi, F., Mantovani, A., Belgiovine, C., & Allavena, P. (2016) · OncoTarget · doi:10.18632/oncotarget.9340 · Cited by 81
Modulation of the CCR6-CCL20 Axis: A Potential Therapeutic Target in Inflammation and Cancer
Ranasinghe, R., & Eri, R. D. (2018) · Medicina · doi:10.3390/medicina54050088 · Cited by 75
TLR1/2 ligand enhances antitumor efficacy of CTLA-4 blockade by increasing intratumoral Treg depletion
Sharma, N., Vacher, J., & Allison, J. P. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1819004116 · Cited by 75
Characteristics and clinical trial results of agonistic anti‑CD40 antibodies in the treatment of malignancies (Review)
Li, D., & Wang, W. (2020) · Oncology Letters · doi:10.3892/ol.2020.12037 · Cited by 73
Involvement of CCR6/CCL20/IL-17 Axis in NSCLC Disease Progression
Kirshberg, S., Izhar, U., Amir, G., Demma, J. A., Vernea, F., Beider, K., Shlomai, Z., Wald, H., Zamir, G. A., Shapira, O. M., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024856 · Cited by 71
Phase I study of ABBV-428, a mesothelin-CD40 bispecific, in patients with advanced solid tumors
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Chirality of TLR-2 ligand Pam3CysSK4 in fully synthetic peptide conjugates critically influences the induction of specific CD8+ T-cells
Khan, S., Weterings, J. J., Britten, C. M., de Jong, A. R., Graafland, D., Melief, C. J. M., van der Burg, S. H., MAREL, G. V. D., Overkleeft, H. S., Filippov, D. V., et al. (2008) · Molecular Immunology · doi:10.1016/j.molimm.2008.10.006 · Cited by 64
CCL 2 as a potential therapeutic target for clear cell renal cell carcinoma
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RRx-001: a systemically non-toxic M2-to-M1 macrophage stimulating and prosensitizing agent in Phase II clinical trials
Oronsky, B. T., Paulmurugan, R., Foygel, K., Scicinski, J. J., Knox, S. J., Peehl, D. M., Zhao, H., Ning, S., Cabrales, P., Summers, T. A., et al. (2016) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2017.1268600 · Cited by 62
Phase I dose‐escalation trial to repurpose propagermanium, an oral CCL2 inhibitor, in patients with breast cancer
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The chemokine receptor CCR6 facilitates the onset of mammary neoplasia in the MMTV-PyMT mouse model via recruitment of tumor-promoting macrophages
Boyle, S. T., Faulkner, J. W., McColl, S. R., & Kochetkova, M. (2015) · Molecular Cancer · doi:10.1186/s12943-015-0394-1 · Cited by 60
Maraviroc
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Initial results from first-in-human study of IPI-549, a tumor macrophage-targeting agent, combined with nivolumab in advanced solid tumors.
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Prognostic role of tumour-associated macrophages and macrophage scavenger receptor 1 in prostate cancer: a systematic review and meta-analysis
Cao, J., Liu, J., Xu, R., Zhu, X., Zhao, X., & Qian, B. (2017) · Oncotarget · doi:10.18632/oncotarget.18743 · Cited by 58
Redox regulation of P-glycoprotein-mediated multidrug resistance in multicellular prostate tumor spheroids
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T-cell-independent Antitumor Effects of CD40 Ligation
Rakhmilevich, A. L., Alderson, K. L., & Sondel, P. M. (2012) · International Reviews of Immunology · doi:10.3109/08830185.2012.698337 · Cited by 56
REPLATINUM Phase III Randomized Study: RRx-001 + Platinum Doublet Versus Platinum Doublet in Third-Line Small Cell Lung Cancer
Oronsky, B. T., Reid, T. R., Larson, C., Caroen, S. Z., Quinn, M. G., Burbano, E., Varner, G., Thilagar, B., Brown, B., Coyle, A., et al. (2019) · Future Oncology · doi:10.2217/fon-2019-0317 · Cited by 56
Zoledronic acid inhibits thyroid cancer stemness and metastasis by repressing M2-like tumor-associated macrophages induced Wnt/β-catenin pathway
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Trabectedin
Allavena, P., Germano, G., Belgiovine, C., D’Incalci, M., & Mantovani, A. (2013) · OncoImmunology · doi:10.4161/onci.24614 · Cited by 55
Advances of CCR5 antagonists: From small molecules to macromolecules
Qi, B., Fang, Q., Liu, S., Hou, W., Li, J., Huang, Y., & Shi, J. (2020) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2020.112819 · Cited by 52
Anibamine, a natural product CCR5 antagonist, as a novel lead for the development of anti-prostate cancer agents
Zhang, X., Haney, K. M., Richardson, A. C., Wilson, E. N., Gewirtz, D. A., Ware, J. L., Zehner, Z. E., & Zhang, Y. (2010) · Bioorganic & Medicinal Chemistry Letters · doi:10.1016/j.bmcl.2010.06.003 · Cited by 51
Small-molecule CSF1R kinase inhibitors; review of patents 2015-present
Denny, W. A., & Flanagan, J. U. (2020) · Expert Opinion on Therapeutic Patents · doi:10.1080/13543776.2021.1839414 · Cited by 51
CD47 Expression Defines Efficacy of Rituximab with CHOP in Non–Germinal Center B-cell (Non-GCB) Diffuse Large B-cell Lymphoma Patients (DLBCL), but Not in GCB DLBCL
Bouwstra, R., He, Y. Z., de Boer, J., Kooistra, H., Cendrowicz, E., Fehrmann, R. S. N., Ammatuna, E., zu Eulenburg, C., Nijland, M., Huls, G. A., et al. (2019) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-18-0781 · Cited by 48
Self-citation
Prognostic value of the expression of C-Chemokine Receptor 6 and 7 and their ligands in non-metastatic breast cancer
Cassier, P. A., Treilleux, I., Bachelot, T., Ray-Coquard, I. L., Bendriss‐Vermare, N., Ménétrier‐Caux, C., Trédan, O., Goddard‐Léon, S., Pin, J., Mignotte, H., et al. (2011) · BMC Cancer · doi:10.1186/1471-2407-11-213 · Cited by 40
Downregulation of CCR5 inhibits the proliferation and invasion of cervical cancer cells and is regulated by microRNA-107
CHE, L.-F., Shao, S.-F., & Wang, L. (2015) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2015.2911 · Cited by 39
Effective antibody therapy induces host-protective antitumor immunity that is augmented by TLR4 agonist treatment
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The CD24+ cell subset promotes invasion and metastasis in human osteosarcoma
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Authors: Cendrowicz, E., Sas, Z., Bremer, E., & Rygiel, T. P.
Affiliations: University Medical Center Groningen (NL)
Medical University of Warsaw (PL)
Corresponding author: Rygiel, Tomasz P.
ORCID: Cendrowicz, Ewa
Sas, Zuzanna
Bremer, Edwin
Rygiel, Tomasz P.
Venue: Cancers
Publisher: MDPI AG
Published: 2021-04-18
Volume: 13
Issue: 8
Pages: 1946
ISSN: 2072-6694 (ISSN-L)
DOI: 10.3390/cancers13081946
PMC: PMC8073377
OpenAlex: W3156547118
Cited by: 332
References: 199
Citations by year: 2026: 33 · 2025: 68 · 2024: 106 · 2023: 72 · 2022: 42 · 2021: 11
FWCI: 5.91
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Cancers (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
Funders: Fundacja na rzecz Nauki Polskiej (TEAM TECH/2016-1/8)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Stress, Anesthesia, and Immune Response
Keywords: tumor-associated macrophages, tumor microenvironment, TAM depletion, TAM reprogramming, tumor immunosuppression, neoangiogenesis, metastasis, antitumor immunity, T cell recruitment

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The Role of Macrophages in Cancer Development and Therapy

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