Tumor-Associated Macrophages: From Mechanisms to Therapy

Noy, Roy; Pollard, Jeffrey W.

doi:10.1016/j.immuni.2014.06.010

Cited by 4,089Immune cells in cancerAngiogenesis and VEGF in CancerCancer Cells and Metastasis

Tumor-Associated Macrophages: From Mechanisms to Therapy

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Noy, Roy, Pollard, Jeffrey W.·2014·Immunity

DOI 10.1016/j.immuni.2014.06.010PMC PMC4137410

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Abstract

The tumor microenvironment is a complex ecology of cells that evolves with and provides support to tumor cells during the transition to malignancy. Among the innate and adaptive immune cells recruited to the tumor site, macrophages are particularly abundant and are present at all stages of tumor progression. Clinical studies and experimental mouse models indicate that these macrophages generally play a protumoral role. In the primary tumor, macrophages can stimulate angiogenesis and enhance tumor cell invasion, motility, and intravasation. During monocytes and/or metastasis, macrophages prime the premetastatic site and promote tumor cell extravasation, survival, and persistent growth. Macrophages are also immunosuppressive, preventing tumor cell attack by natural killer and T cells during tumor progression and after recovery from chemo- or immunotherapy. Therapeutic success in targeting these protumoral roles in preclinical models and in early clinical trials suggests that macrophages are attractive targets as part of combination therapy in cancer treatment.

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TAM-based therapeutic strategies are being developed that aim at TAM targeting, TAM re-education, and TAM depletion.
“Accordingly, TAM-based therapeutic strategies are being developed that aim at TAM targeting, TAM re-education, and TAM depletion [88, 96, 101, 102].”
From Tumor microenvironment complexity and therapeutic implications at a glance (2020) · cites this paper as [88]
Many therapy strategies have attempted to alter the polarization of macrophages or prevent monocyte tumor infiltration.
“Many therapy strategies have attempted to alter the polarization of macrophages’ “re-programming” or prevent monocyte tumor infiltration (Noy and Pollard, 2014).”
From Sysrev: A FAIR Platform for Data Curation and Systematic Evidence Review (2021) · cites this paper as Noy and Pollard, 2014
In preclinical models, macrophages and MDSCs aid tumor growth and metastasis by secreting factors that suppress antitumor immune responses, especially those of CD8+ T cells and NK cells.
“In preclinical models, both of these innate immune cell types aid tumor growth and metastasis through their secretion of factors that suppress antitumor immune responses, especially those of CD8 + T cells and NK cells (166, 167).”
From Immune Checkpoint Inhibitors for the Treatment of Cancer: Clinical Impact and Mechanisms of Response and Resistance (2021) · cites this paper as [167]
Production of CSF-1 by breast cancer cells stimulates recruitment of macrophages to primary breast tumors, leading to TAM secretion of epidermal growth factor, which stimulates invasion and metastasis.
“The production of colony stimulating factor 1 (CSF-1; also known as macrophage colony stimulating factor) by BCCs, has been reported to stimulate the recruitment of macrophages to primary breast tumors, leading to the secretion by tumor-associated macrophages (TAMs) of epidermal growth factor, which binds to its cognate receptor on BCCs to stimulate invasion and metastasis [36–38].”
From The hypoxic tumor microenvironment: A driving force for breast cancer progression (2016) · cites this paper as [38]

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1 retracted

Macrophage Colony-Stimulating Factor Augments Tie2-Expressing Monocyte Differentiation, Angiogenic Function, and Recruitment in a Mouse Model of Breast Cancer
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Arginase I Production in the Tumor Microenvironment by Mature Myeloid Cells Inhibits T-Cell Receptor Expression and Antigen-Specific T-Cell Responses
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Macrophage polarization in tumour progression
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Different Tumor Microenvironments Contain Functionally Distinct Subsets of Macrophages Derived from Ly6C(high) Monocytes
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M1 and M2 Macrophages: Oracles of Health and Disease
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Role of Macrophage Targeting in the Antitumor Activity of Trabectedin
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A Positive Feedback Loop between Mesenchymal-like Cancer Cells and Macrophages Is Essential to Breast Cancer Metastasis
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B7-H4 expression identifies a novel suppressive macrophage population in human ovarian carcinoma
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IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasionPreprint
Gocheva, V., Wang, H., Gadea, B. B., Shree, T., Hunter, K. E., Garfall, A. L., Berman, T. A., & Joyce, J. A. (2010) · Genes & Development · doi:10.1101/gad.1874010 · Cited by 739 · see citing works
Recognition of Human Histocompatibility Leukocyte Antigen (HLA)-E Complexed with HLA Class I Signal Sequence–derived Peptides by CD94/NKG2 Confers Protection from Natural Killer Cell–mediated Lysis
Borrego, F., Ulbrecht, M., Weiss, E. H., Coligan, J. E., & Brööks, A. G. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.187.5.813 · Cited by 726 · cited 1× · see citing works
“…can inhibit the activation of natural killer (NK) cells and a subsets of activated T cells upon their ligation to killer cell immunoglobulin like receptor CD94 (also known asNKG2) (Borrego et al., 1998) or the inhibitory leukocyte immunoglobulin-like receptors LIT-2 (HLA-E and HLA-G respectively).”
Background
A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF- B and enhanced IRF-3/STAT1 activation)
Biswas, S. K. (2005) · Blood · doi:10.1182/blood-2005-01-0428 · Cited by 693 · cited 2× · see citing works
“in vivo both in the primary and metastatic sites (Biswas et al., 2013).”
Background
Cancer-related inflammation: Common themes and therapeutic opportunities
Balkwill, F. R., & Mantovani, A. (2011) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2011.12.005 · Cited by 685 · cited 4× · see citing works
“Furthermore, inflammatory conditions such as Crohn’s disease dramatically increase the risk of colorectal cancer (Balkwill et al., 2005; Balkwill and Mantovani, 2012; Coussens and Werb, 2002; Grivennikov et al., 2010).”
BackgroundInfluential
Origins of tumor-associated macrophages and neutrophils
Cortez‐Retamozo, V., Etzrodt, M., Newton, A., Rauch, P. J., Chudnovskiy, A., Berger, C., Ryan, R. J. H., Iwamoto, Y., Marinelli, B. S., Gorbatov, R., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113744109 · Cited by 680 · cited 3× · see citing works
“probably because the immune system has access to the products of mutated genes and/or recognizes tissue damage caused by invasion (Coussens and Pollard, 2011; Gajewski et al., 2013).”
Background
Reactive nitrogen species in the chemical biology of inflammation
Dedon, P. C., & Tannenbaum, S. R. (2004) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2003.12.017 · Cited by 676 · cited 1× · see citing works
“…can cause tumor initiation by creating a mutagenic microenvironment either directly through free radical generation or indirectly via alterations in the microbiome and barrier functions that allow access of genotoxic bacteria to the epithelial cells (Dedon and Tannenbaum, 2004; Jobin, 2013).”
Background
A Distinct Macrophage Population Mediates Metastatic Breast Cancer Cell Extravasation, Establishment and Growth
Qian, B., Deng, Y., Im, J. H., Muschel, R. J., Zou, Y., Li, J., Lang, R. A., & Pollard, J. W. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006562 · Cited by 664 · cited 2× · see citing works
“Monocytes and/or macrophages are essential metastasis promoters acting both to prepare sites and also to promote the extravasation, survival, and persistent growth of metastatic cells (Joyce and Pollard, 2009; Qian et al., 2009).”
BackgroundSelf-citation
The secreted factors responsible for pre-metastatic niche formation: Old sayings and new thoughts
Peinado, H., Lavotshkin, S., & Lyden, D. C. (2011) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2011.01.002 · Cited by 657 · cited 1× · see citing works
“Exosomes derived from different melanoma strains can also redirect metastatic cell target tropisms from one tissue to another (Peinado et al., 2011).”
Background
Macrophage Expression of Hypoxia-Inducible Factor-1α Suppresses T-Cell Function and Promotes Tumor Progression
Doedens, A. L., Stockmann, C., Rubinstein, M. P., Liao, D., Zhang, N., DeNardo, D. G., Coussens, L. M., Karin, M., Goldrath, A. W., & Johnson, R. S. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-1439 · Cited by 652 · cited 2× · see citing works
“Hypoxia acting via hypoxia inducible factor 1- a (HIF-1a) also induces T cell suppression by TAMS although the mechanism is unknown (Doedens et al., 2010).”
Background
Bv8 regulates myeloid-cell-dependent tumour angiogenesis
Shojaei, F., Wu, X., Zhong, C., Yu, L., Liang, X., Yao, J. J., Blanchard, D., Bais, C., Peale, F. V., Jr., van Bruggen, N., et al. (2007) · Nature · doi:10.1038/nature06348 · Cited by 640 · cited 1× · see citing works
“In other models, M-MDSCs modulate the efficacy of antivascular therapies (Shojaei et al., 2007).”
Background
Targeting the ANG2/TIE2 Axis Inhibits Tumor Growth and Metastasis by Impairing Angiogenesis and Disabling Rebounds of Proangiogenic Myeloid Cells
Mazzieri, R., Pucci, F., Moi, D., Zonari, E., Ranghetti, A., Berti, A., Politi, L. S., Gentner, B., Brown, J. L., Naldini, L., et al. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.02.005 · Cited by 639 · see citing works
Colony-stimulating factor-1 in immunity and inflammation
Chitu, V., & Stanley, E. R. (2006) · Current Opinion in Immunology · doi:10.1016/j.coi.2005.11.006 · Cited by 635 · see citing works
PD-L1 and PD-L2 are differentially regulated by Th1 and Th2 cells
Loke, P., & Allison, J. P. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0931259100 · Cited by 630 · cited 2× · see citing works
“For example, it has been shown that INF-g secretion by activated NK cells that have migrated to the lymph node is an important mediator of CD8+ T cell activation and that HLA-G and HLA-E inhibits this NK cells migration and INF-g secretion (Kelly et al., 2002).”
Background
Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs
Chen, Q., Zhang, X. H.-F., & Massagué, J. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.08.025 · Cited by 619 · see citing works
Tumor-associated macrophages: Functional diversity, clinical significance, and open questions
Biswas, S. K., Allavena, P., & Mantovani, A. (2013) · Seminars in Immunopathology · doi:10.1007/s00281-013-0367-7 · Cited by 551 · cited 1× · see citing works
“Substantial evidence indicates that macrophages, rather than being tumoricidal as suggested after their activation in vitro (Fidler, 1988), adopt a protumoral phenotype in vivo both in the primary and metastatic sites (Biswas et al., 2013).”
Background
Immune Modulation in Cancer with Antibodies
Page, D. B., Postow, M. A., Callahan, M. K., Allison, J. P., & Wolchok, J. D. (2013) · Annual Review of Medicine · doi:10.1146/annurev-med-092012-112807 · Cited by 516 · cited 1× · see citing works
“Exosomes derived from different melanoma strains can also redirect metastatic cell target tropisms from one tissue to another (Peinado et al., 2011).”
Background
l -Arginine Consumption by Macrophages Modulates the Expression of CD3ζ Chain in T Lymphocytes
Rodrı́guez, P. C., Zea, A. H., DeSalvo, J., Culotta, K. S., Zabaleta, J., Quiceno, D. G., Ochoa, J. B., & Ochoa, A. C. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.3.1232 · Cited by 494 · cited 1× · see citing works
“L-arginine is necessary for T cells function, and its depletion inhibits the re-expression of the CD3 z chain after internalization caused by antigen stimulation and TCR signaling (Rodriguez et al., 2003, 2004).”
Background
Leukocyte composition of human breast cancer
Ruffell, B., Au, A., Rugo, H. S., Esserman, L. J., Hwang, E. S., & Coussens, L. M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104303108 · Cited by 481 · cited 1× · see citing works
“In this context and importantly, the combination of macrophages and a high ratio of CD4+ regulatory versus CD8+ T cells in human breast cancer is predictive of poorer survival (Ruffell et al., 2011).”
Background
Tumor-Associated Macrophages Press the Angiogenic Switch in Breast Cancer
Lin, E. Y., & Pollard, J. W. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-0912 · Cited by 463 · cited 1× · see citing works
“Genetic gain-of-function of VEGFA over a loss-of function of CSF1 in the PyMT mouse model also resulted in a dramatic recruitment of macrophages and a rescue of angiogenesis that resulted in an acceleration of tumor progression to malignancy (Lin et al., 2007).”
BackgroundSelf-citation
Gliomas Promote Immunosuppression through Induction of B7-H1 Expression in Tumor-Associated Macrophages
Bloch, O. G., Crane, C. A., Kaur, R., Safaee, M., Rutkowski, M. J., & Parsa, A. T. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-3314 · Cited by 457 · see citing works
Tumor-Infiltrating Monocytic Myeloid-Derived Suppressor Cells Mediate CCR5-Dependent Recruitment of Regulatory T Cells Favoring Tumor Growth
Schlecker, E., Stojanovic, A., Eisen, C., Quack, C., Falk, C. S., Umansky, V., & Cerwenka, A. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1201018 · Cited by 439 · cited 1× · see citing works
“TAMs in this mouse model expressed some of the CCR5 ligands (Schlecker et al., 2012).”
Background
CSF1R inhibition delays cervical and mammary tumor growth in murine models by attenuating the turnover of tumor-associated macrophages and enhancing infiltration by CD8+T cells
Strachan, D. C., Ruffell, B., Oei, Y. A., Bissell, M. J., Coussens, L. M., Pryer, N., & Daniel, D. (2013) · OncoImmunology · doi:10.4161/onci.26968 · Cited by 379 · cited 1× · see citing works
“Similar results can be seen in cervical and breast cancermodels (Strachan et al., 2013).”
Result
Targeting distinct tumor-infiltrating myeloid cells by inhibiting CSF-1 receptor: combating tumor evasion of antiangiogenic therapy
Priceman, S. J., Sung, J. L., Shaposhnik, Z., Burton, J. B., Torres‐Collado, A. X., Moughon, D. L., Johnson, M., Lusis, A. J., Cohen, D. A., Iruela‐Arispe, M. L., et al. (2009) · Blood · doi:10.1182/blood-2009-08-237412 · Cited by 357 · cited 2× · see citing works
“These effects seem not to be restricted to chemotherapy because TIE+ positive TAMs limit the efficacy of antivascular reagents, and their ablation strongly increases the therapeutic efficacy of these agents (Priceman et al., 2010; Welford et al., 2011).”
Background
Induction of tumor-specific T cell memory by NK cell–mediated tumor rejection
Kelly, J. M., Darcy, P. K., Markby, J. L., Godfrey, D. I., Takeda, K., Yagita∥, H., & Smyth, M. J. (2001) · Nature Immunology · doi:10.1038/ni746 · Cited by 356 · cited 2× · see citing works
“For example, it has been shown that INF-g secretion by activated NK cells that have migrated to the lymph node is an important mediator of CD8 T cell activation and that HLA-G and HLA-E inhibits this NK cells migration and INF-g secretion (Kelly et al., 2002).”
Background
Regulation of Adaptive Immunity; The Role of Interleukin-10
Ng, T. H. S., Britton, G. J., Hill, E. V., Verhagen, J., Burton, B. R., & Wraith, D. C. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00129 · Cited by 354 · cited 1× · see citing works
“TGF-b inhibits cytotoxic T lymphocyte, Th1, and Th2 CD4+ T cells (Oh and Li, 2013), whereas IL-10 inhibits Th1 and Th2 CD4+ T cell helper functions (Ng et al., 2013).”
Background
Recruitment of monocytes/macrophages by tissue factor-mediated coagulation is essential for metastatic cell survival and premetastatic niche establishment in mice
Gil‐Bernabé, A. M., Ferjancic, S., Tlalka, M., Zhao, L., Allen, P. D., Im, J. H., Watson, K., Hill, S. A., Amirkhosravi, A., Francis, J. L., et al. (2012) · Blood · doi:10.1182/blood-2011-08-376426 · Cited by 353 · cited 1× · see citing works
“Studies of lung metastasis show that upon their arrival at the target site, tumor cells together with associated platelets recruited via their expression of tissue factor form microclots and arrest in the target tissue vessels (Gil-Bernabé et al., 2012).”
BackgroundSelf-citation
Tumor-associated macrophages: Effectors of angiogenesis and tumor progression
Coffelt, S. B., Hughes, R., & Lewis, C. E. (2009) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2009.02.004 · Cited by 350 · cited 1× · see citing works
“There are numerous additional reports of TAMs affecting angiogenesis in a wide range of models, mostly xenograft ones, and for further information the reader is referred to recent reviews on this topic (Coffelt et al., 2009; Nucera et al., 2011).”
Background
Molecular Pathways: Adipose Inflammation as a Mediator of Obesity-Associated Cancer
Howe, L. R., Subbaramaiah, K., Hudis, C. A., & Dannenberg, A. J. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-2603 · Cited by 343 · see citing works
Marginating Dendritic Cells of the Tumor Microenvironment Cross-Present Tumor Antigens and Stably Engage Tumor-Specific T Cells
Engelhardt, J., Boldajipour, B. A., Beemiller, P., Pandurangi, P., Sorensen, C. M., Werb, Z., Egeblad, M., & Krummel, M. F. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.01.008 · Cited by 330 · see citing works
TGF-β: Guardian of T Cell Function
Oh, S. A., & Li, M. O. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1301843 · Cited by 320 · cited 1× · see citing works
“TGF-b inhibits cytotoxic T lymphocyte, Th1, and Th2 CD4+ T cells (Oh and Li, 2013), whereas IL-10 inhibits Th1 and Th2 CD4+ T cell helper functions (Ng et al., 2013).”
Background
HLA-G1-expressing antigen-presenting cells induce immunosuppressive CD4 + T cells
LeMaoult, J., Krawice-Radanne, I., Dausset, J. B., & Carosella, E. D. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401922101 · Cited by 314 · cited 2× · see citing works
“In addition, HLA-G-transfected APCs can inhibit CD4+ T cell activation and induce immunosuppressive differentiation in vitro (LeMaoult et al., 2004).”
Background
Myeloid Progenitor Cells in the Premetastatic Lung Promote Metastases by Inducing Mesenchymal to Epithelial Transition
Gao, D., Joshi, N., Choi, H., Ryu, S., Hahn, M., Catena, R., Sadik, H., Argani, P., Wagner, P. L., Vahdat, L. T., et al. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-2905 · Cited by 308 · see citing works
Tumor-associated macrophages in breast cancer: distinct subsets, distinct functions
Laoui, D., Movahedi, K., Overmeire, E. V., den Bossche, J. V., Schouppe, E., Mommer, C., Nikolaou, A., Morias, Y., BAETSELIER, P. D., & Ginderachter, J. A. V. (2011) · The International Journal of Developmental Biology · doi:10.1387/ijdb.113371dl · Cited by 304 · see citing works
Macrophage-secreted cytokines drive pancreatic acinar-to-ductal metaplasia through NF-κB and MMPs
Liou, G., Döppler, H. R., Necela, B. M., Krishna, M., Crawford, H. C., Raimondo, M., & Störz, P. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201301001 · Cited by 296 · see citing works
The Macrophage Growth Factor CSF-1 in Mammary Gland Development and Tumor Progression
Lin, E. Y., Gouon–Evans, V., Nguyen, A., & Pollard, J. W. (2002) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1023/a:1020399802795 · Cited by 292 · cited 1× · see citing works
“…in the polarization ofmacrophages by a number of factors including IL-4 synthesized by CD4+ T cells and/or tumor cells (Coussens et al., 2013; Gocheva et al., 2010) and growth factors produced by tumor cells such as colony stimulating factor-1 CSF1 (Lin et al., 2002) and GM-CSF (Su et al., 2014).”
BackgroundSelf-citation
The LILR family: modulators of innate and adaptive immune pathways in health and disease
Brown, D. P., Trowsdale, J., & Allen, R. L. (2004) · Tissue Antigens · doi:10.1111/j.0001-2815.2004.00290.x · Cited by 292 · cited 2× · see citing works
“This Th2 environment is characterized by transforming growth factor-b1 (TGF-b1) and Arginase 1, as well as increased numbers of CD4+ T cells (DeNardo et al., 2009).”
Background
Specific subsets of murine dendritic cells acquire potent T cell regulatory functions following CTLA4-mediated induction of indoleamine 2,3 dioxygenase
Mellor, A. L. (2004) · International Immunology · doi:10.1093/intimm/dxh140 · Cited by 288 · cited 2× · see citing works
“inhibition of T cells but also induces a DCs inhibitory phenotype (Butte et al., 2007; Mellor et al., 2004).”
Background
Intratumoral macrophages contribute to epithelial-mesenchymal transition in solid tumors
Bonde, A.-K., Tischler, V., Kumar, S., Soltermann, A., & Schwendener, R. A. (2012) · BMC Cancer · doi:10.1186/1471-2407-12-35 · Cited by 284 · cited 1× · see citing works
“…SPARC) that increases tumor cell-ECM interaction and thus migration (Sangaletti et al., 2008), Cathepsin proteases that remodel the matrix and release sequestered growth factors (Laoui et al., 2011; Quail and Joyce, 2013) and TGF-b that promotes EMT of the invading tumor cells (Bonde et al., 2012).”
Background
SMAD4-deficient intestinal tumors recruit CCR1+ myeloid cells that promote invasion
Kitamura, T., Kometani, K., Hashida, H., Matsunaga, A., Miyoshi, H., Hosogi, H., Aoki, M., Oshima, M., Hattori, M., Takabayashi, A., et al. (2007) · Nature Genetics · doi:10.1038/ng1997 · Cited by 282 · cited 1× · see citing works
“Furthermore CCL9 acting through its receptor, CCR1, recruits immature myeloid cells in colon cancer models (Kitamura et al., 2010; Kitamura et al., 2007).”
Background
Therapeutic PD-1 Pathway Blockade Augments with Other Modalities of Immunotherapy T-Cell Function to Prevent Immune Decline in Ovarian Cancer
Duraiswamy, J., Freeman, G. J., & Coukos, G. (2013) · Cancer Research · doi:10.1158/0008-5472.can-13-1550 · Cited by 275 · cited 1× · see citing works
“Both PD-L1 and L2 are regulated in TAMs and myeloid-derived suppressor cells (See below—MDSC) (Belai et al., 2014; Duraiswamy et al., 2013).”
Background
Immune regulation by pretenders: cell-to-cell transfers of HLA-G make effector T cells act as regulatory cells
LeMaoult, J., Caumartin, J., Daouya, M., Favier, B., Rond, S. L., González, Á., & Carosella, E. D. (2006) · Blood · doi:10.1182/blood-2006-05-024547 · Cited by 266 · cited 12× · see citing works
“CSF1-regulated macrophages regulate this switch in the PyMT model in part through production of VEGF (Lin and Pollard, 2007).”
BackgroundInfluential
Natural and Induced T Regulatory Cells in Cancer
Adeegbe, D. O., & Nishikawa, H. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00190 · Cited by 248 · cited 2× · see citing works
“Chemokine receptors CCR4, CCR5, CCR6, and CCR10 expressed by nTreg cells are involved in their migration into the tumor microenvironment (Adeegbe and Nishikawa, 2013).”
Background
Tumor-Associated Macrophages Recruit CCR6+ Regulatory T Cells and Promote the Development of Colorectal Cancer via Enhancing CCL20 Production in Mice
Liu, J., Zhang, N., Li, Q., Zhang, W., Fang, K., Leng, Q., Wang, H., Chen, J., & Wang, H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019495 · Cited by 247 · cited 1× · see citing works
“In colorectal cancer, CCL20 secreted by TAMs recruit CCR6+ nTreg cells (Liu et al., 2011).”
Background
Human Anti-Inflammatory Macrophages Induce Foxp3+GITR+CD25+ Regulatory T Cells, Which Suppress via Membrane-Bound TGFβ-1
Savage, N. D. L., de Boer, T., Walburg, K. V., Joosten, S. A., van Meijgaarden, K. E., Geluk, A., & Ottenhoff, T. H. M. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.181.3.2220 · Cited by 235 · cited 1× · see citing works
“Savage and coworkers investigated the ability of human macrophages to induce regulatory T cells and showed that IL-10 expressing anti-inflammatory macrophages but not proinflammatory macrophages are responsible for induction of iTreg cells (Savage et al., 2008).”
Background
Tumor-Associated Macrophages Mediate Immunosuppression in the Renal Cancer Microenvironment by Activating the 15-Lipoxygenase-2 Pathway
Daurkin, I., Eruslanov, E. B., Stoffs, T., Perrin, G. Q., Algood, C. B., Gilbert, S. M., Rosser, C. J., Su, L., Vieweg, J., & Kusmartsev, S. A. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-1261 · Cited by 234 · cited 3× · see citing works
“Several recent studies suggest that such an approach is feasible and therapeutic (Coussens et al., 2013; De Palma and Lewis, 2013).”
Background
TIE2-expressing macrophages limit the therapeutic efficacy of the vascular-disrupting agent combretastatin A4 phosphate in mice
Welford, A. F., Biziato, D., Coffelt, S. B., Nucera, S., Fisher, M. L., Pucci, F., Serio, C. D., Naldini, L., Palma, M. D., Tozer, G. M., et al. (2011) · Journal of Clinical Investigation · doi:10.1172/jci44562 · Cited by 228 · see citing works
A Novel Mouse Model of Inflammatory Bowel Disease Links Mammalian Target of Rapamycin-Dependent Hyperproliferation of Colonic Epithelium to Inflammation-Associated Tumorigenesis
Deng, L., Zhou, J.-F., Sellers, R. S., Li, J.-F., Nguyen, A., Wang, Y., Orlofsky, A., Liu, Q., Hume, D. A., Pollard, J. W., et al. (2009) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090622 · Cited by 228 · see citing works
Self-citation
The interplay between macrophages and angiogenesis in development, tissue injury and regeneration.
Nucera, S., Biziato, D., & de Palma, M. (2011) · International Journal of Developmental Biology · doi:10.1387/ijdb.103227sn · Cited by 221 · cited 1× · see citing works
“There are numerous additional reports of TAMs affecting angiogenesis in a wide range of models, mostly xenograft ones, and for further information the reader is referred to recent reviews on this topic (Coffelt et al., 2009; Nucera et al., 2011).”
Background
Leukocytes in Mammary Development and CancerPreprint
Coussens, L. M., & Pollard, J. W. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a003285 · Cited by 209 · cited 2× · see citing works
“This correlates with enhanced engagement of the acquired immune system indicating antigen recognition probably because the immune system has access to the products of mutated genes and/or recognizes tissue damage caused by invasion (Coussens and Pollard, 2011; Gajewski et al., 2013).”
BackgroundSelf-citation
Macrophage-Derived SPARC Bridges Tumor Cell-Extracellular Matrix Interactions toward Metastasis
Sangaletti, S., Carlo, E. D., Gariboldi, S., Miotti, S., Cappetti, B., Parenza, M., Rumio, C., Brekken, R. A., Chiodoni, C., & Colombo, M. P. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-1327 · Cited by 208 · see citing works
Tumor Microenvironment of Metastasis and Risk of Distant Metastasis of Breast Cancer
Rohan, T. E., Xue, X., Lin, H.-M., D’Alfonso, T. M., Ginter, P. S., Oktay, M. H., Robinson, B. D., Ginsberg, M. S., Gertler, F. B., Glass, A. G., et al. (2014) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/dju136 · Cited by 203 · cited 1× · see citing works
“Importantly, an anatomical structure consisting of macrophages, endothelial, and tumor cells named the tumor microenvironment for metastasis (TMEM) is recognizable in histological sections and is predictive of metastatic potential in primary human breast cancers (Rohan et al., 2014).”
Background
Therapeutic activation of macrophages and microglia to suppress brain tumor-initiating cells
Sarkar, S., Döring, A., Zemp, F. J., Silva, C., Lun, X. Q., Wang, X., Kelly, J. J., Hader, W. J., Hamilton, M. G., Mercier, P., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3597 · Cited by 202 · cited 1× · see citing works
“Similarly, amphotericin B enhances macrophage-mediated inhibition of glioma tumor-initiating cells (Sarkar et al., 2014).”
Background
Myeloid-derived Suppressor Cells in Cancer Patients
Montero, A. J., Diaz-Montero, C. M., Kyriakopoulos, C. E., Bronte, V., & Mandruzzato, S. (2012) · Journal of Immunotherapy · doi:10.1097/cji.0b013e318242169f · Cited by 201 · cited 2× · see citing works
“be further discussed here, and there are excellent reviews defining their functions and classification elsewhere (Gabrilovich andNagaraj, 2009; Gabrilovich et al., 2012;Montero et al., 2012).”
Background
Vascular endothelial growth factor‐induced skin carcinogenesis depends on recruitment and alternative activation of macrophages
Linde, N., Lederle, W., Depner, S., van Rooijen, N., Gutschalk, C. M., & Mueller, M. M. (2012) · The Journal of Pathology · doi:10.1002/path.3989 · Cited by 195 · see citing works
Contribution of the PD‐1 ligands/PD‐1 signaling pathway to dendritic cell‐mediated CD4 + T cell activation
Kuipers, H., Muskens, F., Willart, M. A. M., Hijdra, D., van Assema, F., Coyle, A. J., Hoogsteden, H. C., & Lambrecht, B. N. (2006) · European Journal of Immunology · doi:10.1002/eji.200635978 · Cited by 191 · cited 2× · see citing works
“Indeed, the culture of bonemarrow-derived DCs with anti PD-L1 antibody inhibits their activation, induces IL-10 expression, and suppresses cocultured CD4 T cell activation (Kuipers et al., 2006).”
Background
Myeloid WNT7b Mediates the Angiogenic Switch and Metastasis in Breast Cancer
Yeo, E.-J., Cassetta, L., Qian, B., Lewkowich, I. P., Li, J., Stefater, J. A., Smith, A. N., Wiechmann, L., Wang, Y., Pollard, J. W., et al. (2014) · Cancer Research · doi:10.1158/0008-5472.can-13-2421 · Cited by 190 · cited 1× · see citing works
“In this model, macrophage-synthesized WNT7b targets vascular endothelial cells, stimulating their production of VEGF, resulting in the angiogenic switch (Yeo et al., 2014).”
BackgroundSelf-citation
The role of B7 family molecules in hematologic malignancy
Greaves, P., & Gribben, J. G. (2012) · Blood · doi:10.1182/blood-2012-10-385591 · Cited by 188 · cited 2× · see citing works
“However, it is challenging to determine the specific impact of TAM PD-1 ligand expression on effector cells inhibition in vivo since numerous cells in the tumor microenvironment express PD-L1 (Greaves and Gribben, 2013).”
Background
A clinical study assessing the tolerability and biological effects of infliximab, a TNF-α inhibitor, in patients with advanced cancer
Brown, E. R., Charles, K. A., Hoare, S., Rye, R., Jodrell, D., Aird, R. E., Vora, R., Prabhakar, U., Nakada, M. T., Corringham, R. E., et al. (2008) · Annals of Oncology · doi:10.1093/annonc/mdn054 · Cited by 182 · see citing works
Inactivation of chemokine (C-C motif) receptor 1 (CCR1) suppresses colon cancer liver metastasis by blocking accumulation of immature myeloid cells in a mouse model
Kitamura, T., Fujishita, T., Loetscher, P., Révész, L., Hashida, H., Kizaka‐Kondoh, S., Aoki, M., & Taketo, M. M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002372107 · Cited by 178 · cited 1× · see citing works
“Furthermore CCL9 acting through its receptor, CCR1, recruits immature myeloid cells in colon cancer models (Kitamura et al., 2010; Kitamura et al., 2007).”
Background
Tracking of intertissue migration reveals the origins of tumor-infiltrating monocytes
Shand, F. H. W., Ueha, S., Otsuji, M., Koid, S., Shichino, S., Tsukui, T., Kosugi-Kanaya, M., Abe, J., Tomura, M., Ziogas, J., et al. (2014) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1402914111 · Cited by 173 · cited 2× · see citing works
“…elegant experiments using photoconvertible fluorescent lineage tracing of spleen and BM monocytes suggest that the splenic contribution is minor and that BM is the primary source of monocytes that generate TAMs at least in the Lewis Lung carcinoma syngeneic transplant model (Shand et al., 2014).”
Background
Vascular endothelial growth factor restores delayed tumor progression in tumors depleted of macrophages
Lin, E. Y., Li, J.-F., Bricard, G., Wang, W., Deng, Y., Sellers, R. S., Porcelli, S. A., & Pollard, J. W. (2007) · Molecular Oncology · doi:10.1016/j.molonc.2007.10.003 · Cited by 170 · cited 2× · see citing works
“a loss-of function of CSF1 in the PyMT mouse model also resulted in a dramatic recruitment of macrophages and a rescue of angiogenesis that resulted in an acceleration of tumor progression to malignancy (Lin et al., 2007).”
BackgroundSelf-citation
Tumor-Associated Macrophages in Glioma: Friend or Foe?
Kennedy, B. C., Showers, C. R., Anderson, D. E., Anderson, L., Canoll, P., Bruce, J. N., & Anderson, R. C. E. (2013) · Journal of Oncology · doi:10.1155/2013/486912 · Cited by 164 · cited 1× · see citing works
“TAM expression of B7-1 and B7-2 was shown to be dependent on their activation phenotype; both molecules are expressed by proinflammatory macrophages and are downregulated by antiinflammatory macrophages (Ding et al., 1993; Flores Villanueva et al., 1994; Kennedy et al., 2013).”
Background
Negative co-receptors on lymphocytes
Greenwald, R. J., Latchman, Y. E., & Sharpe, A. H. (2002) · Current Opinion in Immunology · doi:10.1016/s0952-7915(02)00341-2 · Cited by 163 · cited 1× · see citing works
“This differential affinity suggests direct competition for the ligand binding as a mechanism to induce suppression (Greenwald et al., 2002).”
Background
Langerhans Cells Facilitate Epithelial DNA Damage and Squamous Cell Carcinoma
Modi, B. G., Neustadter, J. H., Binda, E., Lewis, J. M., Filler, R. B., Roberts, S. J., Kwong, B. Y., Reddy, S., Overton, J. D., Galan, A., et al. (2012) · Science · doi:10.1126/science.1211600 · Cited by 149 · cited 1× · see citing works
“Consequently, they will not be further discussed here, and there are excellent reviews defining their functions and classification elsewhere (Gabrilovich andNagaraj, 2009; Gabrilovich et al., 2012;Montero et al., 2012).”
Background
Low Surface Expression of B7-1 (CD80) Is an Immunoescape Mechanism of Colon Carcinoma
Tirapu, I., Huarte, E., Guiducci, C., Arina, A., Zaratiegui, M., Murillo, O., González, Á., Berasain, C., Berraondo, P., Fortes, P., et al. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-1681 · Cited by 140 · cited 1× · see citing works
“However, the specific inhibitory effect mediated by TAMs in vivo is still unknown and as with PD1 ligands, CTLA-4 ligands are expressed on some human tumors and other immune cells (Greaves and Gribben, 2013; Tamura et al., 2005; Tirapu et al., 2006).”
Background
Regulation of Macrophage Arginase Expression and Tumor Growth by the Ron Receptor Tyrosine Kinase
Sharda, D. R., Yu, S., Ray, M., Squadrito, M. L., Palma, M. D., Wynn, T. A., Morris, S. M., & Hankey, P. A. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1003460 · Cited by 137 · see citing works
Targeting tumor–stromal interactions in bone metastasis
Esposito, M., & Kang, Y. (2013) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.10.006 · Cited by 129 · cited 1× · see citing works
“Because this process is dependent on a different cell type to classical macrophages it will not be reviewed further here, but readers are referred to recent reviews that discuss the process and therapeutic opportunities (Camacho and Pienta, 2014; Esposito and Kang, 2014; Mundy, 2002).”
Background
Expression of Functional B7-H2 and B7.2 Costimulatory Molecules and Their Prognostic Implications inDe novoAcute Myeloid Leukemia
Tamura, H., Dan, K., Tamada, K., Nakamura, K., Shioi, Y., Hyodo, H., Wang, S.-D., Dong, H., Chen, L., & Ogata, K. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-04-2672 · Cited by 119 · cited 1× · see citing works
“However, the specific inhibitory effect mediated by TAMs in vivo is still unknown and as with PD1 ligands, CTLA-4 ligands are expressed on some human tumors and other immune cells (Greaves and Gribben, 2013; Tamura et al., 2005; Tirapu et al., 2006).”
Background
Human Neuroblastoma Cells Trigger an Immunosuppressive Program in Monocytes by Stimulating Soluble HLA-G Release
Morandi, F., Levreri, I., Bocca, P., Galleni, B., Raffaghello, L., Ferrone, S., Prigione, I., & Pistoia, V. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-4588 · Cited by 113 · cited 11× · see citing works
“These HLA-G negative tumors might rely on myeloid cell 52 Immunity 41, July 17, 2014 ª2014 Elsevier Inc. HLA-G expression as an effector of inhibitory mechanisms.”
BackgroundInfluential
CD8+ Tumor-Infiltrating T Cells Are Trapped in the Tumor-Dendritic Cell Network
Boissonnas, A., Licata, F., Poupel, L., Jacquelin, S., Fetler, L., Krumeich, S., Théry, C., Amigorena, S., & Combadière, C. (2013) · Neoplasia · doi:10.1593/neo.121572 · Cited by 107 · cited 2× · see citing works
“chemotherapy, suggesting an immunosuppressive mechanism (Boissonnas et al., 2013; Engelhardt et al., 2012).”
Background
Tumor Progression Stage and Anatomical Site Regulate Tumor-Associated Macrophage and Bone Marrow-Derived Monocyte Polarization
Redente, E. F., Dwyer‐Nield, L. D., Merrick, D., Raina, K., Agarwal, R., Pao, W. J., Rice, P. L., Shroyer, K. R., & Malkinson, A. M. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090879 · Cited by 94 · see citing works
Regulation of T helper cell responses in experimental murine schistosomiasis by IL-10. Effect on expression of B7 and B7-2 costimulatory molecules by macrophages.
Flores-Villanueva, P. O., Reiser, H., & Stadecker, M. J. (1994) · The Journal of Immunology · doi:10.4049/jimmunol.153.11.5190 · Cited by 94 · cited 1× · see citing works
“TAM expression of B7-1 and B7-2 was shown to be dependent on their activation phenotype; both molecules are expressed by proinflammatory macrophages and are downregulated by antiinflammatory macrophages (Ding et al., 1993; Flores Villanueva et al., 1994; Kennedy et al., 2013).”
Background
VCAM-1 and VAP-1 recruit myeloid cells that promote pulmonary metastasis in mice
Ferjancic, S., Gil‐Bernabé, A. M., Hill, S. A., Allen, P. D., Richardson, P., Sparey, T. J., Savory, E., McGuffog, J., & Muschel, R. J. (2013) · Blood · doi:10.1182/blood-2012-08-449819 · Cited by 90 · cited 1× · see citing works
“In addition, clotting upregulates VECM1 on endothelial cells that promote myeloid cell attachment and thus their recruitment (Ferjan ci c et al., 2013).”
Background
Colorectal Cancer: Looking for Answers in the Microbiota
Jobin, C. (2013) · Cancer Discovery · doi:10.1158/2159-8290.cd-13-0042 · Cited by 89 · see citing works
Recombinant HLA-G5 and -G6 drive U937 myelomonocytic cell production of TGF-β1
McIntire, R. H., Morales, P. J., Petroff, M. G., Colonna, M., & Hunt, J. S. (2004) · Journal of Leukocyte Biology · doi:10.1189/jlb.0604337 · Cited by 79 · cited 1× · see citing works
“Monocytes and macrophages can themselves express members of the LILRB inhibitory receptors family (LIT-2 and LIT-4) that upon binding HLA-G causes them to acquire immunosuppressive phenotype through the secretion of IL-10 and TGF-b1 (Brown et al., 2004;McIntire et al., 2004).”
Background
Stromal cell‐derived CSF‐1 blockade prolongs xenograft survival of CSF‐1‐negative neuroblastoma
Abraham, D., Zins, K., Sioud, M., Lucas, T., Schäfer, R., Stanley, E. R., & Aharinejad, S. (2009) · International Journal of Cancer · doi:10.1002/ijc.24859 · Cited by 75 · cited 2× · see citing works
“affected tumor malignancy in both xenograft and GEM models of cancer (Abraham et al., 2010; Lin et al., 2001; Qian and Pollard, 2010; Quail and Joyce, 2013).”
Background
Production of immune-modulatory nonclassical molecules HLA-G and HLA-E by tumor infiltrating ameboid microglia/macrophages in glioblastomas: A role in innate immunity?
Křen, L., Múčková, K., Lžičařová, E., Sova, M., Vybíhal, V., Svoboda, T., Fadrus, P., Smrčka, M., Slabý, O., Lakomý, R., et al. (2010) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2010.01.014 · Cited by 57 · see citing works
The clinical significance of inflammatory cytokines in primary cell culture in endometrial carcinoma
Smith, H. O., Stephens, N. D., Qualls, C., Fligelman, T., Wang, T., Lin, C., Burton, E. M., Griffith, J. K., & Pollard, J. W. (2012) · Molecular Oncology · doi:10.1016/j.molonc.2012.07.002 · Cited by 57 · see citing works
Self-citation
PD-1 blockage delays murine squamous cell carcinoma development
Belai, E. B., de Oliveira, C. E., Gasparoto, T. H., Ramos, R. N., Torres, S. A., Garlet, G. P., Cavassani, K. A., Silva, J. S., & Campanelli, A. P. (2013) · Carcinogenesis · doi:10.1093/carcin/bgt305 · Cited by 46 · cited 1× · see citing works
“Both PD-L1 and L2 are regulated in TAMs and myeloid-derived suppressor cells (See below—MDSC) (Belai et al., 2014; Duraiswamy et al., 2013).”
Background
Increased B7-H1 and B7-H4 Expressions on Circulating Monocytes and Tumor-Associated Macrophages are Involved in Immune Evasion in Patients with Gastric Cancer.
Matsunaga, T., Saito, H., & Ikeguchi, M. (2011) · Europe PMC (PubMed Central) · Cited by 29 · see citing works
Increase of Circulating B7-H4–Expressing CD68+ Macrophage Correlated With Clinical Stage of Lung Carcinomas
Chen, C., Zhu, Y.-B., Shen, Y., Zhu, Y., Zhang, X., & Huang, J.-A. (2012) · Journal of Immunotherapy · doi:10.1097/cji.0b013e31824212c4 · Cited by 27 · cited 1× · see citing works
“In addition, the expression of B7-H4 on TAMs was found to correlate with clinical stage of lung carcinoma and gastric cancer (Chen et al., 2012; Matsunaga et al., 2011).”
Background
Increased B7-H1 and B7-H4 expressions on circulating monocytes and tumor-associated macrophages are involved in immune evasion in patients with gastric cancer
松永, 知. (2011) · Tottori University research result repository (Tottori University) · Cited by 22 · see citing works
A multi-targeted approach to treating bone metastases
Camacho, D. F., & Pienta, K. J. (2014) · Cancer and Metastasis Reviews · doi:10.1007/s10555-013-9476-y · Cited by 16 · cited 1× · see citing works
“Because this process is dependent on a different cell type to classical macrophages it will not be reviewed further here, but readers are referred to recent reviews that discuss the process and therapeutic opportunities (Camacho and Pienta, 2014; Esposito and Kang, 2014; Mundy, 2002).”
Background
Macrophage Therapy of Cancer Metastasis
Fidler, I. J. (2007) · Novartis Foundation symposium · doi:10.1002/9780470513736.ch12 · Cited by 15 · cited 1× · see citing works
“Substantial evidence indicates that macrophages, rather than being tumoricidal as suggested after their activation in vitro (Fidler, 1988), adopt a protumoral phenotype in vivo both in the primary and metastatic sites (Biswas et al., 2013).”
Background

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Tumour-associated macrophages as treatment targets in oncology
Mantovani, A., Marchesi, F., Malesci, A., Laghi, L., & Allavena, P. (2017) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2016.217 · Cited by 4,065 · see citing works
Wound Healing: A Cellular Perspective.
Rodrigues, M., Kosaric, N., Bonham, C., & Gurtner, G. (2019) · Physiological Reviews · doi:10.1152/physrev.00067.2017 · Cited by 2,752 · see citing works
Inflammation and tumor progression: signaling pathways and targeted intervention
Zhao, H., Wu, L., Yan, G., Chen, Y., Zhou, M., Wu, Y., & Li, Y. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00658-5 · Cited by 2,907 · see citing works
Macrophage Polarization
Murray, P. J. (2017) · Annual Review of Physiology · doi:10.1146/annurev-physiol-022516-034339 · Cited by 2,981 · see citing works
Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver
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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
EMT, CSCs, and drug resistance: the mechanistic link and clinical implications
Shibue, T., & Weinberg, R. A. (2017) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2017.44 · Cited by 2,539 · see citing works
Macrophages as regulators of tumour immunity and immunotherapy
DeNardo, D. G., & Ruffell, B. (2019) · Nature reviews. Immunology · doi:10.1038/s41577-019-0127-6 · Cited by 2,542 · see citing works
Immune Checkpoint Inhibitors for the Treatment of Cancer: Clinical Impact and Mechanisms of Response and Resistance
Bagchi, S., Yuan, R., & Engleman, E. G. (2021) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathol-042020-042741 · Cited by 2,189 · see citing works
Macrophages in immunoregulation and therapeutics
Chen, S., Saeed, A. F. U. H., Liu, Q., Jiang, Q., Xu, H., Xiao, G. G., Rao, L., & Duo, Y. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01452-1 · Cited by 2,348 · see citing works
Roles of the immune system in cancer: From tumor initiation to metastatic progression
Gonzalez, H., Hagerling, C., & Werb, Z. (2018) · Genes & Development · doi:10.1101/gad.314617.118 · Cited by 2,111 · see citing works
The evolving landscape of biomarkers for checkpoint inhibitor immunotherapy
Havel, J. J., Chowell, D., & Chan, T. A. (2019) · Nature Reviews Cancer · doi:10.1038/s41568-019-0116-x · Cited by 2,286 · see citing works
Targeting macrophages: therapeutic approaches in cancer
Cassetta, L., & Pollard, J. W. (2018) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2018.169 · Cited by 2,057 · see citing works
Self-citation
Tumor microenvironment as a therapeutic target in cancer
Xiao, Y. Q., & Yu, D. (2020) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2020.107753 · Cited by 1,977 · see citing works
NK Cells Stimulate Recruitment of cDC1 into the Tumor Microenvironment Promoting Cancer Immune Control
Böttcher, J. P., Bonavita, E., Chakravarty, P., Blees, H., Cabeza-Cabrerizo, M., Sammicheli, S., Rogers, N. C., Sahai, E., Zelenay, S., & Reis e Sousa, C. (2018) · Cell · doi:10.1016/j.cell.2018.01.004 · Cited by 1,857 · see citing works
Neutrophils in cancer: Neutral no more
Coffelt, S. B., Wellenstein, M. D., & de Visser, K. E. (2016) · Nature reviews. Cancer · doi:10.1038/nrc.2016.52 · Cited by 1,830 · see citing works
Tumor-Associated Macrophages in Tumor Immunity
Pan, Y., Yu, Y., Wang, X., & Zhang, T. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.583084 · Cited by 1,884 · see citing works
Tumor microenvironment complexity and therapeutic implications at a glance
Baghban, R., Roshangar, L., Jahanban-Esfahlan, R., Seidi, K., Ebrahimi-Kalan, A., Jaymand, M., Kolahian, S., Javaheri, T., & Zare, P. (2020) · Cell Communication and Signaling · doi:10.1186/s12964-020-0530-4 · Cited by 1,784 · see citing works
“Accordingly, TAM-based therapeutic strategies are being developed that aim at TAM targeting, TAM reeducation, and TAM depletion [88, 96, 101, 102] .”
Background
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
The role of ROS in tumour development and progression
Cheung, E. C., & Vousden, K. H. (2022) · Nature reviews. Cancer · doi:10.1038/s41568-021-00435-0 · Cited by 1,623 · see citing works
Antiangiogenesis Strategies Revisited: From Starving Tumors to Alleviating Hypoxia
Jain, R. K. (2014) · Cancer Cell · doi:10.1016/j.ccell.2014.10.006 · Cited by 1,589 · see citing works
Human chimeric antigen receptor macrophages for cancer immunotherapy
Klichinsky, M., Ruella, M., Shestova, O., Lu, X. M., Best, A., Zeeman, M., Schmierer, M., Gabrusiewicz, K., Anderson, N. R., Petty, N. E., et al. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0462-y · Cited by 1,495 · see citing works
Tumor-associated macrophages in tumor metastasis: biological roles and clinical therapeutic applications
Lin, Y., Xu, J., & Lan, H. (2019) · Journal of Hematology & Oncology · doi:10.1186/s13045-019-0760-3 · Cited by 1,398 · see citing works
Extracellular Vesicles: Unique Intercellular Delivery Vehicles
Maas, S. L. N., Breakefield, X. O., & Weaver, A. M. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2016.11.003 · Cited by 1,419 · see citing works
The Cancer Stem Cell Niche: How Essential Is the Niche in Regulating Stemness of Tumor Cells?
Plaks, V., Kong, N., & Werb, Z. (2015) · Cell Stem Cell · doi:10.1016/j.stem.2015.02.015 · Cited by 1,557 · see citing works
Macrophages and Therapeutic Resistance in Cancer
Ruffell, B., & Coussens, L. M. (2015) · Cancer Cell · doi:10.1016/j.ccell.2015.02.015 · Cited by 1,474 · see citing works
Cellular Senescence: Aging, Cancer, and Injury
Calcinotto, A., Kohli, J., Zagato, E., Pellegrini, L., Demaria, M., & Alimonti, A. (2019) · Physiological Reviews · doi:10.1152/physrev.00020.2018 · Cited by 1,270 · see citing works
Block copolymer micelles in nanomedicine applications
Cabral, H., Miyata, K., Osada, K., & Kataoka, K. (2018) · Chemical Reviews · doi:10.1021/acs.chemrev.8b00199 · Cited by 1,309 · see citing works
Metabolism via Arginase or Nitric Oxide Synthase: Two Competing Arginine Pathways in Macrophages
Rath, M., ller, I. M. ⁄., Kropf, P., Closs, E. I., & Munder, M. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00532 · Cited by 1,271 · see citing works
Therapeutic developments in pancreatic cancer: current and future perspectives
Neoptolemos, J. P., Kleeff, J., Michl, P., Costello, E., Greenhalf, W., & Palmer, D. H. (2018) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-018-0005-x · Cited by 1,170 · see citing works
Targeting Tumor Microenvironment for Cancer Therapy
Roma-Rodrigues, C., Mendes, R., Baptista, P. V., & Fernandes, A. R. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20040840 · Cited by 1,187 · see citing works
Immune cell promotion of metastasis
Kitamura, T., Qian, B.-Z., & Pollard, J. W. (2015) · Nature Reviews Immunology · doi:10.1038/nri3789 · Cited by 1,158 · see citing works
Self-citation
Tumor-associated macrophages: an accomplice in solid tumor progression
Chen, Y., Song, Y., Du, W., Gong, L., Chang, H., & Zou, Z. (2019) · Journal of Biomedical Science · doi:10.1186/s12929-019-0568-z · Cited by 1,096 · see citing works
Immunological hallmarks of stromal cells in the tumour microenvironment
Turley, S. J., Cremasco, V., & Astarita, J. L. (2015) · Nature Reviews Immunology · doi:10.1038/nri3902 · Cited by 1,140 · see citing works
Single-cell RNA-seq enables comprehensive tumour and immune cell profiling in primary breast cancer
Chung, W., Eum, H. H., Lee, H.-O., Lee, K.-M., Lee, H.-B., Kim, K.-T., Ryu, H. S., Kim, S., Lee, J. E., Park, Y. H., et al. (2017) · Nature Communications · doi:10.1038/ncomms15081 · Cited by 992 · see citing works
“Previous reports suggest that TAMs may show an immunosuppressive M2 signature, which promotes tumorigenesis by suppressing immune surveillance and inducing angiogenesis, rather than the activating M1-type signature 45 .”
Influential
Radiotherapy and immunotherapy: a beneficial liaison?
Weichselbaum, R. R., Liang, H. L., Deng, L., & Fu, Y. (2017) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2016.211 · Cited by 1,073 · see citing works
Autophagy, ferroptosis, pyroptosis, and necroptosis in tumor immunotherapy
Gao, W., Wang, Y., Zhou, Y., Wang, X., & Yu, Y. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01046-3 · Cited by 1,069 · see citing works
Interrogation of the Microenvironmental Landscape in Brain Tumors Reveals Disease-Specific Alterations of Immune Cells
Klemm, F., Maas, R. R., Bowman, R. L., Kornete, M., Soukup, K., Nassiri, S., Brouland, J., Iacobuzio–Donahue, C. A., Brennan, C. W., Tabar, V. S., et al. (2020) · Cell · doi:10.1016/j.cell.2020.05.007 · Cited by 1,050 · see citing works
CD8+ T cell differentiation and dysfunction in cancer
Philip, M., & Schietinger, A. (2022) · Nature Reviews Immunology · doi:10.1038/s41577-021-00574-3 · Cited by 1,052 · see citing works
Colony-stimulating factor 1 receptor (CSF1R) inhibitors in cancer therapy
Cannarile, M. A., Weisser, M., Jacob, W., Jegg, A.-M., Ries, C. H., & Rüttinger, D. (2017) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-017-0257-y · Cited by 1,029 · 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
Developmental and Functional Heterogeneity of Monocytes
Guilliams, M., Mildner, A., & Yona, S. (2018) · Immunity · doi:10.1016/j.immuni.2018.10.005 · Cited by 973 · see citing works
Targeting tumor-associated macrophages in cancer
Pathria, P., Louis, T. L., & Varner, J. A. (2019) · Trends in Immunology · doi:10.1016/j.it.2019.02.003 · Cited by 933 · see citing works
Tumor immune microenvironment characterization in clear cell renal cell carcinoma identifies prognostic and immunotherapeutically relevant messenger RNA signatures
Şenbabaoğlu, Y., Gejman, R. S., Winer, A. G., Liu, M., Allen, E. M. V., de Velasco, G., Miao, D., Ostrovnaya, I., Drill, E. N., Luna, A., et al. (2016) · Genome biology · doi:10.1186/s13059-016-1092-z · Cited by 949 · see citing works
Nanoparticle design strategies for enhanced anticancer therapy by exploiting the tumour microenvironment
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Macrophages: Development and Tissue Specialization
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Targeted delivery of a PD-1-blocking scFv by CAR-T cells enhances anti-tumor efficacy in vivo
Rafiq, S., Yeku, O. O., Jackson, H. J., Purdon, T. J., van Leeuwen, D. G., Drakes, D. J., Song, M., Miele, M. M., Li, Z., Wang, P., et al. (2018) · Nature Biotechnology · doi:10.1038/nbt.4195 · Cited by 833 · see citing works
The role of myeloid cells in cancer therapies
Engblom, C., Pfirschke, C., & Pittet, M. J. (2016) · Nature Reviews Cancer · doi:10.1038/nrc.2016.54 · Cited by 788 · see citing works
The Role of Cancer-Associated Fibroblasts and Fibrosis in Liver Cancer
Affo, S., Yu, L.-X., & Schwabe, R. F. (2017) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathol-052016-100322 · Cited by 757 · see citing works
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Authors: Noy, R., & Pollard, J. W.
Affiliations: Albert Einstein College of Medicine (US)
Corresponding author: Pollard, Jeffrey W.
ORCID: Noy, Roy
Pollard, Jeffrey W.
Venue: Immunity
Publisher: Elsevier BV
Published: 2014-07
Volume: 41
Issue: 1
Pages: 49-61
ISSN: 1074-7613 (ISSN-L)
DOI: 10.1016/j.immuni.2014.06.010
PMC: PMC4137410
OpenAlex: W1971620413
Cited by: 4,089
References: 136
Citations by year: 2026: 258 · 2025: 326 · 2024: 359 · 2023: 393 · 2022: 485 · 2021: 479 · 2020: 424 · 2019: 379 · 2018: 297 · 2017: 285 · 2016: 215 · 2015: 157 · 2014: 27 · 2013: 3 · 2012: 1
FWCI: 22.25
Type: journal article
Language: en
Update notices: erratum (2014-11-20)
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 381 d)
Locations: Immunity (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Wellcome Trust (101067, 101067/Z/13/Z)
National Institutes of Health (UL1TR001073)
National Cancer Institute (P01CA100324, R01CA172451)
National Center for Advancing Translational Sciences
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
Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Keywords: tumor-associated macrophages, tumor microenvironment, tumor angiogenesis, tumor invasion, metastasis, pre-metastatic niche, immunosuppression, natural killer cells, T cells, macrophage-targeted therapy, combination cancer therapy
MeSH terms: Animals, Cell Movement, Cell Survival, Cell Transformation, Neoplastic, Humans, Immunosuppression Therapy, Macrophages, Neoplasm Invasiveness, Neoplasm Metastasis, Neoplasms, Neovascularization, Pathologic, Cell Lineage, Cell Proliferation, Mice, Tumor Microenvironment

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Tumor-Associated Macrophages: From Mechanisms to Therapy

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