Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Role of Biological Mediators of Tumor-Associated Macrophages in Breast Cancer Progression

Author(s): Yan Li, Kumar Ganesan and Jianping Chen*

Volume 29, Issue 33, 2022

Published on: 27 July, 2022

Page: [5420 - 5440] Pages: 21

DOI: 10.2174/0929867329666220520121711

Price: $65

Abstract

Background: Breast cancer (BRCA) has become the most common cancer worldwide. The tumor microenvironment (TME) in the breast exerts a crucial role in promoting BRCA initiation, progression, and metastasis. Tumor-associated macrophages (TAMs) are the primary component of tumor-infiltrating immune cells through biological mediators that convert TME into malignant tumors. Combinations of these biological mediators can promote tumor growth, metastasis, angiogenesis, and immune suppression and limit the anti-tumor activity of conventional chemotherapy and radiotherapy.

Objectives: The present study aimed to highlight the functions of several biological mediators in the breast thatgenerate TME into malignant tumors. Furthermore, this review offers a rationale for TAM-targeted therapy as a novel treatment strategy for BRCA.

Results: This review emphasizes TAM-associated biological mediators of TME, viz., cancer- associated fibroblasts, endothelial cells, adipocytes, tumor-derived exosomes, extracellular matrix, and other immune cells, which facilitate TME in malignant tumors. Evidence suggests that the increased infiltration of TAMs and elevated expression of TAMrelated genes are associated with a poor prognosis of BRCA. Based on these findings, TAM-targeted therapeutic strategies, including inhibitors of CSF-1/CSF-1R, CCL2/CCR2, CCL5-CCR5, bisphosphonate, nanoparticle, and exosomal-targeted delivery have been developed, and are currently being employed in intervention trials.

Conclusion: This review concludes the roles of biological mediators of TME that interact with TAMs in BRCA, providing a rationale for TAM-targeted therapy as a novel treatment approach for BRCA.

Keywords: Tumor-associated macrophages, biological mediators, tumor microenvironment, breast cancer, TAMtargeted therapy, breast cancer.

[1]
Harbeck, N.; Penault-Llorca, F.; Cortes, J.; Gnant, M.; Houssami, N.; Poortmans, P.; Ruddy, K.; Tsang, J.; Cardoso, F. Breast cancer. Nat. Rev. Dis. Primers, 2019, 5(1), 66.
[http://dx.doi.org/10.1038/s41572-019-0111-2] [PMID: 31548545]
[2]
Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2018, 68(6), 394-424.
[http://dx.doi.org/10.3322/caac.21492] [PMID: 30207593]
[3]
Ferlay, J.; Colombet, M.; Soerjomataram, I.; Parkin, D.M.; Piñeros, M.; Znaor, A.; Bray, F. Cancer statistics for the year 2020: An overview. Int. J. Cancer, 2021, 149(4), 778-789.
[http://dx.doi.org/10.1002/ijc.33588] [PMID: 33818764]
[4]
Malherbe, K. Tumor microenvironment and the role of artificial intelligence in breast cancer detection and prognosis. Am. J. Pathol., 2021, 191(8), 1364-1373.
[http://dx.doi.org/10.1016/j.ajpath.2021.01.014] [PMID: 33639101]
[5]
Naito, Y.; Yoshioka, Y.; Yamamoto, Y.; Ochiya, T. How cancer cells dictate their microenvironment: Present roles of extracellular vesicles. Cell. Mol. Life Sci., 2017, 74(4), 697-713.
[http://dx.doi.org/10.1007/s00018-016-2346-3] [PMID: 27582126]
[6]
Liu, Y.; Shi, K.; Chen, Y.; Wu, X.; Chen, Z.; Cao, K.; Tao, Y.; Chen, X.; Liao, J.; Zhou, J. Exosomes and their role in cancer progression. Front. Oncol., 2021, 11, 639159.
[http://dx.doi.org/10.3389/fonc.2021.639159] [PMID: 33828985]
[7]
Choi, J.; Gyamfi, J.; Jang, H.; Koo, J.S. The role of tumor-associated macrophage in breast cancer biology. Histol. Histopathol., 2018, 33(2), 133-145.
[PMID: 28681373]
[8]
Derks, S.; de Klerk, L.K.; Xu, X.; Fleitas, T.; Liu, K.X.; Liu, Y.; Dietlein, F.; Margolis, C.; Chiaravalli, A.M.; Da Silva, A.C.; Ogino, S.; Akarca, F.G.; Freeman, G.J.; Rodig, S.J.; Hornick, J.L.; van Allen, E.; Li, B.; Liu, S.X.; Thorsson, V.; Bass, A.J. Characterizing diversity in the tumor-immune microenvironment of distinct subclasses of gastroesophageal adenocarcinomas. Ann. Oncol., 2020, 31(8), 1011-1020.
[http://dx.doi.org/10.1016/j.annonc.2020.04.011] [PMID: 32387455]
[9]
Condeelis, J.; Pollard, J.W. Macrophages: Obligate partners for tumor cell migration, invasion, and metastasis. Cell, 2006, 124(2), 263-266.
[http://dx.doi.org/10.1016/j.cell.2006.01.007] [PMID: 16439202]
[10]
Dong, F.; Ruan, S.; Wang, J.; Xia, Y.; Le, K.; Xiao, X.; Hu, T.; Wang, Q. M2 macrophage-induced lncRNA PCAT6 facilitates tumorigenesis and angiogenesis of triple-negative breast cancer through modulation of VEGFR2. Cell Death Dis., 2020, 11(9), 728.
[http://dx.doi.org/10.1038/s41419-020-02926-8] [PMID: 32908134]
[11]
Sainz, B., Jr; Carron, E.; Vallespinós, M.; Machado, H.L. Cancer stem cells and macrophages: Implications in tumor biology and therapeutic strategies. Mediators Inflamm., 2016, 2016, 9012369.
[http://dx.doi.org/10.1155/2016/9012369] [PMID: 26980947]
[12]
Mantovani, A.; Sozzani, S.; Locati, M.; Allavena, P.; Sica, A. Macrophage polarization: Tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol., 2002, 23(11), 549-555.
[http://dx.doi.org/10.1016/S1471-4906(02)02302-5] [PMID: 12401408]
[13]
Nienhuis, H.H.; Gaykema, S.B.; Timmer-Bosscha, H.; Jalving, M.; Brouwers, A.H.; Lub-de Hooge, M.N.; van der Vegt, B.; Overmoyer, B.; de Vries, E.G.; Schröder, C.P. Targeting breast cancer through its microenvironment: Current status of preclinical and clinical research in finding relevant targets. Pharmacol. Ther., 2015, 147, 63-79.
[http://dx.doi.org/10.1016/j.pharmthera.2014.11.004] [PMID: 25444756]
[14]
Ostuni, R.; Kratochvill, F.; Murray, P.J.; Natoli, G. Macrophages and cancer: From mechanisms to therapeutic implications. Trends Immunol., 2015, 36(4), 229-239.
[http://dx.doi.org/10.1016/j.it.2015.02.004] [PMID: 25770924]
[15]
Squadrito, M.L.; De Palma, M. Macrophage regulation of tumor angiogenesis: Implications for cancer therapy. Mol. Aspects Med., 2011, 32(2), 123-145.
[http://dx.doi.org/10.1016/j.mam.2011.04.005] [PMID: 21565215]
[16]
Chanmee, T.; Ontong, P.; Konno, K.; Itano, N. Tumor-associated macrophages as major players in the tumor microenvironment. Cancers (Basel), 2014, 6(3), 1670-1690.
[http://dx.doi.org/10.3390/cancers6031670] [PMID: 25125485]
[17]
DeNardo, D.G.; Barreto, J.B.; Andreu, P.; Vasquez, L.; Tawfik, D.; Kolhatkar, N.; Coussens, L.M. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell, 2009, 16(2), 91-102.
[http://dx.doi.org/10.1016/j.ccr.2009.06.018] [PMID: 19647220]
[18]
Sousa, S.; Brion, R.; Lintunen, M.; Kronqvist, P.; Sandholm, J.; Mönkkönen, J.; Kellokumpu-Lehtinen, P.L.; Lauttia, S.; Tynninen, O.; Joensuu, H.; Heymann, D.; Määttä, J.A. Human breast cancer cells educate macrophages toward the M2 activation status. Breast Cancer Res., 2015, 17(1), 101.
[http://dx.doi.org/10.1186/s13058-015-0621-0] [PMID: 26243145]
[19]
Sica, A.; Larghi, P.; Mancino, A.; Rubino, L.; Porta, C.; Totaro, M.G.; Rimoldi, M.; Biswas, S.K.; Allavena, P.; Mantovani, A. Macrophage polarization in tumour progression. Semin. Cancer Biol., 2008, 18(5), 349-355.
[http://dx.doi.org/10.1016/j.semcancer.2008.03.004] [PMID: 18467122]
[20]
Tang, X. Tumor-associated macrophages as potential diagnostic and prognostic biomarkers in breast cancer. Cancer Lett., 2013, 332(1), 3-10.
[http://dx.doi.org/10.1016/j.canlet.2013.01.024] [PMID: 23348699]
[21]
Gil, Z.; Billan, S. Crosstalk between macrophages and endothelial cells in the tumor microenvironment. Mol. Ther., 2021, 29(3), 895-896.
[http://dx.doi.org/10.1016/j.ymthe.2021.02.002] [PMID: 33600771]
[22]
DeNardo, D.G.; Brennan, D.J.; Rexhepaj, E.; Ruffell, B.; Shiao, S.L.; Madden, S.F.; Gallagher, W.M.; Wadhwani, N.; Keil, S.D.; Junaid, S.A.; Rugo, H.S.; Hwang, E.S.; Jirström, K.; West, B.L.; Coussens, L.M. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov., 2011, 1(1), 54-67.
[http://dx.doi.org/10.1158/2159-8274.CD-10-0028] [PMID: 22039576]
[23]
Tiainen, S.; Masarwah, A.; Oikari, S.; Rilla, K.; Hämäläinen, K.; Sudah, M.; Sutela, A.; Vanninen, R.; Ikonen, J.; Tammi, R.; Tammi, M.; Auvinen, P. Tumor microenvironment and breast cancer survival: Combined effects of breast fat, M2 macrophages and hyaluronan create a dismal prognosis. Breast Cancer Res. Treat., 2020, 179(3), 565-575.
[http://dx.doi.org/10.1007/s10549-019-05491-7] [PMID: 31720917]
[24]
Qian, B.Z.; Pollard, J.W. Macrophage diversity enhances tumor progression and metastasis. Cell, 2010, 141(1), 39-51.
[http://dx.doi.org/10.1016/j.cell.2010.03.014] [PMID: 20371344]
[25]
Qiu, S-Q.; Waaijer, S.J.H.; Zwager, M.C.; de Vries, E.G.E.; van der Vegt, B.; Schröder, C.P. Tumor-associated macrophages in breast cancer: Innocent bystander or important player? Cancer Treat. Rev., 2018, 70, 178-189.
[http://dx.doi.org/10.1016/j.ctrv.2018.08.010] [PMID: 30227299]
[26]
Lin, Y.; Xu, J.; Lan, H. Tumor-associated macrophages in tumor metastasis: Biological roles and clinical therapeutic applications. J. Hematol. Oncol., 2019, 12(1), 76.
[http://dx.doi.org/10.1186/s13045-019-0760-3] [PMID: 31300030]
[27]
Lin, E.Y.; Li, J.F.; Gnatovskiy, L.; Deng, Y.; Zhu, L.; Grzesik, D.A.; Qian, H.; Xue, X.N.; Pollard, J.W. Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res., 2006, 66(23), 11238-11246.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-1278] [PMID: 17114237]
[28]
Ries, C.H.; Cannarile, M.A.; Hoves, S.; Benz, J.; Wartha, K.; Runza, V.; Rey-Giraud, F.; Pradel, L.P.; Feuerhake, F.; Klaman, I.; Jones, T.; Jucknischke, U.; Scheiblich, S.; Kaluza, K.; Gorr, I.H.; Walz, A.; Abiraj, K.; Cassier, P.A.; Sica, A.; Gomez-Roca, C.; de Visser, K.E.; Italiano, A.; Le Tourneau, C.; Delord, J.P.; Levitsky, H.; Blay, J.Y.; Rüttinger, D. Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell, 2014, 25(6), 846-859.
[http://dx.doi.org/10.1016/j.ccr.2014.05.016] [PMID: 24898549]
[29]
Soria, G.; Ben-Baruch, A. The inflammatory chemokines CCL2 and CCL5 in breast cancer. Cancer Lett., 2008, 267(2), 271-285.
[http://dx.doi.org/10.1016/j.canlet.2008.03.018] [PMID: 18439751]
[30]
Svensson, S.; Abrahamsson, A.; Rodriguez, G.V.; Olsson, A.K.; Jensen, L.; Cao, Y.; Dabrosin, C. CCL2 and CCL5 are novel therapeutic targets for estrogen-dependent breast cancer. Clin. Cancer Res., 2015, 21(16), 3794-3805.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-0204] [PMID: 25901081]
[31]
Qian, B.Z.; Li, J.; Zhang, H.; Kitamura, T.; Zhang, J.; Campion, L.R.; Kaiser, E.A.; Snyder, L.A.; Pollard, J.W. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature, 2011, 475(7355), 222-225.
[http://dx.doi.org/10.1038/nature10138] [PMID: 21654748]
[32]
Kitamura, T.; Qian, B.Z.; Soong, D.; Cassetta, L.; Noy, R.; Sugano, G.; Kato, Y.; Li, J.; Pollard, J.W. CCL2-induced chemokine cascade promotes breast cancer metastasis by enhancing retention of metastasis-associated macrophages. J. Exp. Med., 2015, 212(7), 1043-1059.
[http://dx.doi.org/10.1084/jem.20141836] [PMID: 26056232]
[33]
Bonapace, L.; Coissieux, M.M.; Wyckoff, J.; Mertz, K.D.; Varga, Z.; Junt, T.; Bentires-Alj, M. Cessation of CCL2 inhibition accelerates breast cancer metastasis by promoting angiogenesis. Nature, 2014, 515(7525), 130-133.
[http://dx.doi.org/10.1038/nature13862] [PMID: 25337873]
[34]
Erin, N.; Grahovac, J.; Brozovic, A.; Efferth, T. Tumor microenvironment and epithelial mesenchymal transition as targets to overcome tumor multidrug resistance. Drug Resist. Updat., 2020, 53, 100715.
[http://dx.doi.org/10.1016/j.drup.2020.100715] [PMID: 32679188]
[35]
Reed, J.R.; Stone, M.D.; Beadnell, T.C.; Ryu, Y.; Griffin, T.J.; Schwertfeger, K.L. Fibroblast growth factor receptor 1 activation in mammary tumor cells promotes macrophage recruitment in a CX3CL1-dependent manner. PLoS One, 2012, 7(9), e45877.
[http://dx.doi.org/10.1371/journal.pone.0045877] [PMID: 23029290]
[36]
Boyle, S.T.; Faulkner, J.W.; McColl, S.R.; Kochetkova, M. The chemokine receptor CCR6 facilitates the onset of mammary neoplasia in the MMTV-PyMT mouse model via recruitment of tumor-promoting macrophages. Mol. Cancer, 2015, 14(1), 115.
[http://dx.doi.org/10.1186/s12943-015-0394-1] [PMID: 26047945]
[37]
Karnoub, A.E.; Dash, A.B.; Vo, A.P.; Sullivan, A.; Brooks, M.W.; Bell, G.W.; Richardson, A.L.; Polyak, K.; Tubo, R.; Weinberg, R.A. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature, 2007, 449(7162), 557-563.
[http://dx.doi.org/10.1038/nature06188] [PMID: 17914389]
[38]
Katanov, C.; Lerrer, S.; Liubomirski, Y.; Leider-Trejo, L.; Meshel, T.; Bar, J.; Feniger-Barish, R.; Kamer, I.; Soria-Artzi, G.; Kahani, H.; Banerjee, D.; Ben-Baruch, A. Regulation of the inflammatory profile of stromal cells in human breast cancer: Prominent roles for TNF-α and the NF-κB pathway. Stem Cell Res. Ther., 2015, 6(1), 87.
[http://dx.doi.org/10.1186/s13287-015-0080-7] [PMID: 25928089]
[39]
Yoshimura, T.; Howard, O.M.; Ito, T.; Kuwabara, M.; Matsukawa, A.; Chen, K.; Liu, Y.; Liu, M.; Oppenheim, J.J.; Wang, J.M. Monocyte chemoattractant protein-1/CCL2 produced by stromal cells promotes lung metastasis of 4T1 murine breast cancer cells. PLoS One, 2013, 8(3), e58791.
[http://dx.doi.org/10.1371/journal.pone.0058791] [PMID: 23527025]
[40]
Adair-Kirk, T.L.; Senior, R.M. Fragments of extracellular matrix as mediators of inflammation. Int. J. Biochem. Cell Biol., 2008, 40(6-7), 1101-1110.
[http://dx.doi.org/10.1016/j.biocel.2007.12.005] [PMID: 18243041]
[41]
O’Brien, J.; Lyons, T.; Monks, J.; Lucia, M.S.; Wilson, R.S.; Hines, L.; Man, Y.G.; Borges, V.; Schedin, P. Alternatively activated macrophages and collagen remodeling characterize the postpartum involuting mammary gland across species. Am. J. Pathol., 2010, 176(3), 1241-1255.
[http://dx.doi.org/10.2353/ajpath.2010.090735] [PMID: 20110414]
[42]
Schwertfeger, K.L.; Cowman, M.K.; Telmer, P.G.; Turley, E.A.; McCarthy, J.B. Hyaluronan, inflammation, and breast cancer progression. Front. Immunol., 2015, 6, 236.
[http://dx.doi.org/10.3389/fimmu.2015.00236] [PMID: 26106384]
[43]
Kobayashi, N.; Miyoshi, S.; Mikami, T.; Koyama, H.; Kitazawa, M.; Takeoka, M.; Sano, K.; Amano, J.; Isogai, Z.; Niida, S.; Oguri, K.; Okayama, M.; McDonald, J.A.; Kimata, K.; Taniguchi, S.; Itano, N. Hyaluronan deficiency in tumor stroma impairs macrophage trafficking and tumor neovascularization. Cancer Res., 2010, 70(18), 7073-7083.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-4687] [PMID: 20823158]
[44]
Insua-Rodríguez, J.; Oskarsson, T. The extracellular matrix in breast cancer. Adv. Drug Deliv. Rev., 2016, 97, 41-55.
[http://dx.doi.org/10.1016/j.addr.2015.12.017] [PMID: 26743193]
[45]
Green, K.A.; Lund, L.R. ECM degrading proteases and tissue remodelling in the mammary gland. BioEssays, 2005, 27(9), 894-903.
[http://dx.doi.org/10.1002/bies.20281] [PMID: 16108064]
[46]
Ruffell, B.; Coussens, L.M. Macrophages and therapeutic resistance in cancer. Cancer Cell, 2015, 27(4), 462-472.
[http://dx.doi.org/10.1016/j.ccell.2015.02.015] [PMID: 25858805]
[47]
Pittet, M.J. Behavior of immune players in the tumor microenvironment. Curr. Opin. Oncol., 2009, 21(1), 53-59.
[http://dx.doi.org/10.1097/CCO.0b013e32831bc38a] [PMID: 19125019]
[48]
Marigo, I.; Trovato, R.; Hofer, F.; Ingangi, V.; Desantis, G.; Leone, K.; De Sanctis, F.; Ugel, S.; Canè, S.; Simonelli, A.; Lamolinara, A.; Iezzi, M.; Fassan, M.; Rugge, M.; Boschi, F.; Borile, G.; Eisenhaure, T.; Sarkizova, S.; Lieb, D.; Hacohen, N.; Azzolin, L.; Piccolo, S.; Lawlor, R.; Scarpa, A.; Carbognin, L.; Bria, E.; Bicciato, S.; Murray, P.J.; Bronte, V. Disabled homolog 2 controls prometastatic activity of tumor-associated macrophages. Cancer Discov., 2020, 10(11), 1758-1773.
[http://dx.doi.org/10.1158/2159-8290.CD-20-0036] [PMID: 32651166]
[49]
Gratchev, A.; Guillot, P.; Hakiy, N.; Politz, O.; Orfanos, C.E.; Schledzewski, K.; Goerdt, S. Alternatively activated macrophages differentially express fibronectin and its splice variants and the extracellular matrix protein betaIG-H3. Scand. J. Immunol., 2001, 53(4), 386-392.
[http://dx.doi.org/10.1046/j.1365-3083.2001.00885.x] [PMID: 11285119]
[50]
Schnoor, M.; Cullen, P.; Lorkowski, J.; Stolle, K.; Robenek, H.; Troyer, D.; Rauterberg, J.; Lorkowski, S. Production of type VI collagen by human macrophages: A new dimension in macrophage functional heterogeneity. J. Immunol., 2008, 180(8), 5707-5719.
[http://dx.doi.org/10.4049/jimmunol.180.8.5707] [PMID: 18390756]
[51]
Karousou, E.; D’Angelo, M.L.; Kouvidi, K.; Vigetti, D.; Viola, M.; Nikitovic, D.; De Luca, G.; Passi, A. Collagen VI and hyaluronan: The common role in breast cancer. BioMed Res. Int., 2014, 2014, 606458.
[http://dx.doi.org/10.1155/2014/606458] [PMID: 25126569]
[52]
Joyce, J.A.; Pollard, J.W. Microenvironmental regulation of metastasis. Nat. Rev. Cancer, 2009, 9(4), 239-252.
[http://dx.doi.org/10.1038/nrc2618] [PMID: 19279573]
[53]
Liguori, M.; Solinas, G.; Germano, G.; Mantovani, A.; Allavena, P. Tumor-associated macrophages as incessant builders and destroyers of the cancer stroma. Cancers (Basel), 2011, 3(4), 3740-3761.
[http://dx.doi.org/10.3390/cancers3043740] [PMID: 24213109]
[54]
Chen, J.; Yao, Y.; Gong, C.; Yu, F.; Su, S.; Chen, J.; Liu, B.; Deng, H.; Wang, F.; Lin, L.; Yao, H.; Su, F.; Anderson, K.S.; Liu, Q.; Ewen, M.E.; Yao, X.; Song, E. CCL18 from tumor-associated macrophages promotes breast cancer metastasis via PITPNM3. Cancer Cell, 2011, 19(4), 541-555.
[http://dx.doi.org/10.1016/j.ccr.2011.02.006] [PMID: 21481794]
[55]
Su, S.; Liao, J.; Liu, J.; Huang, D.; He, C.; Chen, F.; Yang, L.; Wu, W.; Chen, J.; Lin, L.; Zeng, Y.; Ouyang, N.; Cui, X.; Yao, H.; Su, F.; Huang, J.D.; Lieberman, J.; Liu, Q.; Song, E. Blocking the recruitment of naive CD4+ T cells reverses immunosuppression in breast cancer. Cell Res., 2017, 27(4), 461-482.
[http://dx.doi.org/10.1038/cr.2017.34] [PMID: 28290464]
[56]
Trikha, P.; Sharma, N.; Pena, C.; Reyes, A.; Pécot, T.; Khurshid, S.; Rawahneh, M.; Moffitt, J.; Stephens, J.A.; Fernandez, S.A.; Ostrowski, M.C.; Leone, G. E2f3 in tumor macrophages promotes lung metastasis. Oncogene, 2016, 35(28), 3636-3646.
[http://dx.doi.org/10.1038/onc.2015.429] [PMID: 26549026]
[57]
Linde, N.; Casanova-Acebes, M.; Sosa, M.S.; Mortha, A.; Rahman, A.; Farias, E.; Harper, K.; Tardio, E.; Reyes Torres, I.; Jones, J.; Condeelis, J.; Merad, M.; Aguirre-Ghiso, J.A. Macrophages orchestrate breast cancer early dissemination and metastasis. Nat. Commun., 2018, 9(1), 21.
[http://dx.doi.org/10.1038/s41467-017-02481-5] [PMID: 29295986]
[58]
Yang, M.; Ma, B.; Shao, H.; Clark, A.M.; Wells, A. Macrophage phenotypic subtypes diametrically regulate epithelial-mesenchymal plasticity in breast cancer cells. BMC Cancer, 2016, 16(1), 419.
[http://dx.doi.org/10.1186/s12885-016-2411-1] [PMID: 27387344]
[59]
Sanderson, R.D.; Elkin, M.; Rapraeger, A.C.; Ilan, N.; Vlodavsky, I. Heparanase regulation of cancer, autophagy and inflammation: New mechanisms and targets for therapy. FEBS J., 2017, 284(1), 42-55.
[http://dx.doi.org/10.1111/febs.13932] [PMID: 27758044]
[60]
El-Nadi, M.; Hassan, H.; Saleh, M.E.; Nassar, E.; Ismail, Y.M.; Amer, M.; Greve, B.; Götte, M.; El-Shinawi, M.; Ibrahim, S.A. Induction of heparanase via IL-10 correlates with a high infiltration of CD163+ M2-type tumor-associated macrophages in inflammatory breast carcinomas. Matrix Biol. Plus, 2020, 6-7, 100030.
[http://dx.doi.org/10.1016/j.mbplus.2020.100030] [PMID: 33543027]
[61]
Cheng, N.; Bei, Y.; Song, Y.; Zhang, W.; Xu, L.; Zhang, W.; Yang, N.; Bai, X.; Shu, Y.; Shen, P. B7-H3 augments the pro-angiogenic function of tumor-associated macrophages and acts as a novel adjuvant target for triple-negative breast cancer therapy. Biochem. Pharmacol., 2021, 183, 114298.
[http://dx.doi.org/10.1016/j.bcp.2020.114298] [PMID: 33153969]
[62]
Larsen, A.M.H.; Kuczek, D.E.; Kalvisa, A.; Siersbæk, M.S.; Thorseth, M.L.; Johansen, A.Z.; Carretta, M.; Grøntved, L.; Vang, O.; Madsen, D.H. Collagen density modulates the immunosuppressive functions of macrophages. J. Immunol., 2020, 205(5), 1461-1472.
[http://dx.doi.org/10.4049/jimmunol.1900789] [PMID: 32839214]
[63]
Burke, R.M.; Madden, K.S.; Perry, S.W.; Zettel, M.L.; Brown, E.B., III Tumor-associated macrophages and stromal TNF-α regulate collagen structure in a breast tumor model as visualized by second harmonic generation. J. Biomed. Opt., 2013, 18(8), 86003.
[http://dx.doi.org/10.1117/1.JBO.18.8.086003] [PMID: 23912760]
[64]
Kuang, D.M.; Wu, Y.; Chen, N.; Cheng, J.; Zhuang, S.M.; Zheng, L. Tumor-derived hyaluronan induces formation of immunosuppressive macrophages through transient early activation of monocytes. Blood, 2007, 110(2), 587-595.
[http://dx.doi.org/10.1182/blood-2007-01-068031] [PMID: 17395778]
[65]
Acerbi, I.; Cassereau, L.; Dean, I.; Shi, Q.; Au, A.; Park, C.; Chen, Y.Y.; Liphardt, J.; Hwang, E.S.; Weaver, V.M. Human breast cancer invasion and aggression correlates with ECM stiffening and immune cell infiltration. Integr. Biol., 2015, 7(10), 1120-1134.
[http://dx.doi.org/10.1039/c5ib00040h] [PMID: 25959051]
[66]
Nurmik, M.; Ullmann, P.; Rodriguez, F.; Haan, S.; Letellier, E. In search of definitions: Cancer-associated fibroblasts and their markers. Int. J. Cancer, 2020, 146(4), 895-905.
[http://dx.doi.org/10.1002/ijc.32193] [PMID: 30734283]
[67]
Aboussekhra, A. Role of cancer-associated fibroblasts in breast cancer development and prognosis. Int. J. Dev. Biol., 2011, 55(7-9), 841-849.
[http://dx.doi.org/10.1387/ijdb.113362aa] [PMID: 22161840]
[68]
Yu, Y.; Xiao, C.H.; Tan, L.D.; Wang, Q.S.; Li, X.Q.; Feng, Y.M. Cancer-associated fibroblasts induce epithelial-mesenchymal transition of breast cancer cells through paracrine TGF-β signalling. Br. J. Cancer, 2014, 110(3), 724-732.
[http://dx.doi.org/10.1038/bjc.2013.768] [PMID: 24335925]
[69]
Bu, L.; Baba, H.; Yoshida, N.; Miyake, K.; Yasuda, T.; Uchihara, T.; Tan, P.; Ishimoto, T. Biological heterogeneity and versatility of cancer-associated fibroblasts in the tumor microenvironment. Oncogene, 2019, 38(25), 4887-4901.
[http://dx.doi.org/10.1038/s41388-019-0765-y] [PMID: 30816343]
[70]
Kuen, J.; Darowski, D.; Kluge, T.; Majety, M. Pancreatic cancer cell/fibroblast co-culture induces M2 like macrophages that influence therapeutic response in a 3D model. PLoS One, 2017, 12(7), e0182039.
[http://dx.doi.org/10.1371/journal.pone.0182039] [PMID: 28750018]
[71]
Shelton, M.; Anene, C.A.; Nsengimana, J.; Roberts, W.; Newton-Bishop, J.; Boyne, J.R. The role of CAF derived exosomal microRNAs in the tumour microenvironment of melanoma. Biochim. Biophys. Acta Rev. Cancer, 2021, 1875(1), 188456.
[http://dx.doi.org/10.1016/j.bbcan.2020.188456] [PMID: 33153973]
[72]
Ksiazkiewicz, M.; Gottfried, E.; Kreutz, M.; Mack, M.; Hofstaedter, F.; Kunz-Schughart, L.A. Importance of CCL2-CCR2A/2B signaling for monocyte migration into spheroids of breast cancer-derived fibroblasts. Immunobiology, 2010, 215(9-10), 737-747.
[http://dx.doi.org/10.1016/j.imbio.2010.05.019] [PMID: 20605053]
[73]
Zhou, J.; Wang, X.H.; Zhao, Y.X.; Chen, C.; Xu, X.Y.; Sun, Q.; Wu, H.Y.; Chen, M.; Sang, J.F.; Su, L.; Tang, X.Q.; Shi, X.B.; Zhang, Y.; Yu, Q.; Yao, Y.Z.; Zhang, W.J. Cancer-associated fibroblasts correlate with tumor-associated macrophages infiltration and lymphatic metastasis in triple negative breast cancer patients. J. Cancer, 2018, 9(24), 4635-4641.
[http://dx.doi.org/10.7150/jca.28583] [PMID: 30588247]
[74]
Ziani, L.; Chouaib, S.; Thiery, J. Alteration of the antitumor immune response by cancer-associated fibroblasts. Front. Immunol., 2018, 9, 414.
[http://dx.doi.org/10.3389/fimmu.2018.00414] [PMID: 29545811]
[75]
Khalid, A.; Wolfram, J.; Ferrari, I.; Mu, C.; Mai, J.; Yang, Z.; Zhao, Y.; Ferrari, M.; Ma, X.; Shen, H. Recent advances in discovering the role of CCL5 in metastatic breast cancer. Mini Rev. Med. Chem., 2015, 15(13), 1063-1072.
[http://dx.doi.org/10.2174/138955751513150923094709] [PMID: 26420723]
[76]
Allaoui, R.; Bergenfelz, C.; Mohlin, S.; Hagerling, C.; Salari, K.; Werb, Z.; Anderson, R.L.; Ethier, S.P.; Jirström, K.; Påhlman, S.; Bexell, D.; Tahin, B.; Johansson, M.E.; Larsson, C.; Leandersson, K. Cancer-associated fibroblast-secreted CXCL16 attracts monocytes to promote stroma activation in triple-negative breast cancers. Nat. Commun., 2016, 7(1), 13050.
[http://dx.doi.org/10.1038/ncomms13050] [PMID: 27725631]
[77]
Salimifard, S.; Masjedi, A.; Hojjat-Farsangi, M.; Ghalamfarsa, G.; Irandoust, M.; Azizi, G.; Mohammadi, H.; Keramati, M.R.; Jadidi-Niaragh, F. Cancer associated fibroblasts as novel promising therapeutic targets in breast cancer. Pathol. Res. Pract., 2020, 216(5), 152915.
[http://dx.doi.org/10.1016/j.prp.2020.152915] [PMID: 32146002]
[78]
Mazur, A.; Holthoff, E.; Vadali, S.; Kelly, T.; Post, S.R. Cleavage of type I collagen by fibroblast activation protein-α enhances class A scavenger receptor mediated macrophage adhesion. PLoS One, 2016, 11(3), e0150287.
[http://dx.doi.org/10.1371/journal.pone.0150287] [PMID: 26934296]
[79]
Liao, D.; Luo, Y.; Markowitz, D.; Xiang, R.; Reisfeld, R.A. Cancer associated fibroblasts promote tumor growth and metastasis by modulating the tumor immune microenvironment in a 4T1 murine breast cancer model. PLoS One, 2009, 4(11), e7965.
[http://dx.doi.org/10.1371/journal.pone.0007965] [PMID: 19956757]
[80]
Gok Yavuz, B.; Gunaydin, G.; Gedik, M.E.; Kosemehmetoglu, K.; Karakoc, D.; Ozgur, F.; Guc, D. Cancer associated fibroblasts sculpt tumour microenvironment by recruiting monocytes and inducing immunosuppressive PD-1+ TAMs. Sci. Rep., 2019, 9(1), 3172.
[http://dx.doi.org/10.1038/s41598-019-39553-z] [PMID: 30816272]
[81]
Stüber, T.; Monjezi, R.; Wallstabe, L.; Kühnemundt, J.; Nietzer, S.L.; Dandekar, G.; Wöckel, A.; Einsele, H.; Wischhusen, J.; Hudecek, M. Inhibition of TGF-β-receptor signaling augments the antitumor function of ROR1-specific CAR T-cells against triple-negative breast cancer. J. Immunother. Cancer, 2020, 8(1), e000676.
[http://dx.doi.org/10.1136/jitc-2020-000676] [PMID: 32303620]
[82]
Hargadon, K.M. Dysregulation of TGFβ1 Activity in cancer and its influence on the quality of anti-tumor immunity. J. Clin. Med., 2016, 5(9), 76.
[http://dx.doi.org/10.3390/jcm5090076] [PMID: 27589814]
[83]
Kalluri, R.; Zeisberg, M. Fibroblasts in cancer. Nat. Rev. Cancer, 2006, 6(5), 392-401.
[http://dx.doi.org/10.1038/nrc1877] [PMID: 16572188]
[84]
Bohrer, L.R.; Schwertfeger, K.L. Macrophages promote fibroblast growth factor receptor-driven tumor cell migration and invasion in a CXCR2-dependent manner. Mol. Cancer Res., 2012, 10(10), 1294-1305.
[http://dx.doi.org/10.1158/1541-7786.MCR-12-0275] [PMID: 22893608]
[85]
Cohen, N.; Shani, O.; Raz, Y.; Sharon, Y.; Hoffman, D.; Abramovitz, L.; Erez, N. Fibroblasts drive an immunosuppressive and growth-promoting microenvironment in breast cancer via secretion of Chitinase 3-like 1. Oncogene, 2017, 36(31), 4457-4468.
[http://dx.doi.org/10.1038/onc.2017.65] [PMID: 28368410]
[86]
Baig, M.S.; Roy, A.; Rajpoot, S.; Liu, D.; Savai, R.; Banerjee, S.; Kawada, M.; Faisal, S.M.; Saluja, R.; Saqib, U.; Ohishi, T.; Wary, K.K. Tumor-derived exosomes in the regulation of macrophage polarization. Inflamm. Res., 2020, 69(5), 435-451.
[http://dx.doi.org/10.1007/s00011-020-01318-0] [PMID: 32162012]
[87]
Sen, K.; Sheppe, A.E.F.; Singh, I.; Hui, W.W.; Edelmann, M.J.; Rinaldi, C. Exosomes released by breast cancer cells under mild hyperthermic stress possess immunogenic potential and modulate polarization in vitro in macrophages. Int. J. Hyperthermia, 2020, 37(1), 696-710.
[http://dx.doi.org/10.1080/02656736.2020.1778800] [PMID: 32568583]
[88]
Chow, A.; Zhou, W.; Liu, L.; Fong, M.Y.; Champer, J.; Van Haute, D.; Chin, A.R.; Ren, X.; Gugiu, B.G.; Meng, Z.; Huang, W.; Ngo, V.; Kortylewski, M.; Wang, S.E. Macrophage immunomodulation by breast cancer-derived exosomes requires Toll-like receptor 2-mediated activation of NF-κB. Sci. Rep., 2014, 4(1), 5750.
[http://dx.doi.org/10.1038/srep05750] [PMID: 25034888]
[89]
Ham, S.; Lima, L.G.; Chai, E.P.Z.; Muller, A.; Lobb, R.J.; Krumeich, S.; Wen, S.W.; Wiegmans, A.P.; Möller, A. Breast cancer-derived exosomes alter macrophage polarization via gp130/STAT3 signaling. Front. Immunol., 2018, 9, 871.
[http://dx.doi.org/10.3389/fimmu.2018.00871] [PMID: 29867925]
[90]
Piao, Y.J.; Kim, H.S.; Hwang, E.H.; Woo, J.; Zhang, M.; Moon, W.K. Breast cancer cell-derived exosomes and macrophage polarization are associated with lymph node metastasis. Oncotarget, 2017, 9(7), 7398-7410.
[http://dx.doi.org/10.18632/oncotarget.23238] [PMID: 29484119]
[91]
Biswas, S.; Mandal, G.; Roy Chowdhury, S.; Purohit, S.; Payne, K.K.; Anadon, C.; Gupta, A.; Swanson, P.; Yu, X.; Conejo-Garcia, J.R.; Bhattacharyya, A. Exosomes produced by mesenchymal stem cells drive differentiation of myeloid cells into immunosuppressive M2-Polarized macrophages in breast cancer. J. Immunol., 2019, 203(12), 3447-3460.
[http://dx.doi.org/10.4049/jimmunol.1900692] [PMID: 31704881]
[92]
Shi, S.Z.; Lee, E.J.; Lin, Y.J.; Chen, L.; Zheng, H.Y.; He, X.Q.; Peng, J.Y.; Noonepalle, S.K.; Shull, A.Y.; Pei, F.C.; Deng, L.B.; Tian, X.L.; Deng, K.Y.; Shi, H.; Xin, H.B. Recruitment of monocytes and epigenetic silencing of intratumoral CYP7B1 primarily contribute to the accumulation of 27-hydroxycholesterol in breast cancer. Am. J. Cancer Res., 2019, 9(10), 2194-2208.
[PMID: 31720082]
[93]
Gajeton, J.; Krukovets, I.; Muppala, S.; Verbovetskiy, D.; Zhang, J.; Stenina-Adognravi, O. Hyperglycemia-induced miR-467 drives Tumor Inflammation and Growth in Breast Cancer. Cancers (Basel), 2021, 13(6), 1346.
[http://dx.doi.org/10.3390/cancers13061346] [PMID: 33809756]
[94]
Moradi-Chaleshtori, M.; Bandehpour, M.; Heidari, N.; Mohammadi-Yeganeh, S.; Mahmoud Hashemi, S. Exosome-mediated miR-33 transfer induces M1 polarization in mouse macrophages and exerts antitumor effect in 4T1 breast cancer cell line. Int. Immunopharmacol., 2021, 90, 107198.
[http://dx.doi.org/10.1016/j.intimp.2020.107198] [PMID: 33249048]
[95]
Guo, J.; Duan, Z.; Zhang, C.; Wang, W.; He, H.; Liu, Y.; Wu, P.; Wang, S.; Song, M.; Chen, H.; Chen, C.; Si, Q.; Xiang, R.; Luo, Y. Mouse 4T1 breast cancer cell-derived exosomes induce proinflammatory cytokine production in macrophages via miR-183. J. Immunol., 2020, 205(10), 2916-2925.
[http://dx.doi.org/10.4049/jimmunol.1901104] [PMID: 32989094]
[96]
Yu, X.; Zhang, Q.; Zhang, X.; Han, Q.; Li, H.; Mao, Y.; Wang, X.; Guo, H.; Irwin, D.M.; Niu, G.; Tan, H. Exosomes from macrophages exposed to apoptotic breast cancer cells promote breast cancer proliferation and metastasis. J. Cancer, 2019, 10(13), 2892-2906.
[http://dx.doi.org/10.7150/jca.31241] [PMID: 31281466]
[97]
Chen, W.X.; Wang, D.D.; Zhu, B.; Zhu, Y.Z.; Zheng, L.; Feng, Z.Q.; Qin, X.H. Exosomal miR-222 from adriamycin-resistant MCF-7 breast cancer cells promote macrophages M2 polarization via PTEN/Akt to induce tumor progression. Aging (Albany NY), 2021, 13(7), 10415-10430.
[http://dx.doi.org/10.18632/aging.202802] [PMID: 33752173]
[98]
Yang, M.; Chen, J.; Su, F.; Yu, B.; Su, F.; Lin, L.; Liu, Y.; Huang, J.D.; Song, E. Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol. Cancer, 2011, 10(1), 117.
[http://dx.doi.org/10.1186/1476-4598-10-117] [PMID: 21939504]
[99]
Yao, X.; Tu, Y.; Xu, Y.; Guo, Y.; Yao, F.; Zhang, X. Endoplasmic reticulum stress-induced exosomal miR-27a-3p promotes immune escape in breast cancer via regulating PD-L1 expression in macrophages. J. Cell. Mol. Med., 2020, 24(17), 9560-9573.
[http://dx.doi.org/10.1111/jcmm.15367] [PMID: 32672418]
[100]
Jang, J.Y.; Lee, J.K.; Jeon, Y.K.; Kim, C.W. Exosome derived from epigallocatechin gallate treated breast cancer cells suppresses tumor growth by inhibiting tumor-associated macrophage infiltration and M2 polarization. BMC Cancer, 2013, 13(1), 421.
[http://dx.doi.org/10.1186/1471-2407-13-421] [PMID: 24044575]
[101]
Calder, P.C.; Kew, S. The immune system: A target for functional foods? Br. J. Nutr., 2002, 88(S2)(Suppl. 2), S165-S177.
[http://dx.doi.org/10.1079/BJN2002682] [PMID: 12495459]
[102]
Jiang, P.; Gao, W.; Ma, T.; Wang, R.; Piao, Y.; Dong, X.; Wang, P.; Zhang, X.; Liu, Y.; Su, W.; Xiang, R.; Zhang, J.; Li, N. CD137 promotes bone metastasis of breast cancer by enhancing the migration and osteoclast differentiation of monocytes/macrophages. Theranostics, 2019, 9(10), 2950-2966.
[http://dx.doi.org/10.7150/thno.29617] [PMID: 31244935]
[103]
Kim, E.Y.; Choi, B.; Kim, J.E.; Park, S.O.; Kim, S.M.; Chang, E.J. Interleukin-22 mediates the chemotactic migration of breast cancer cells and macrophage infiltration of the bone microenvironment by potentiating S1P/SIPR signaling. Cells, 2020, 9(1), E131.
[http://dx.doi.org/10.3390/cells9010131] [PMID: 31935914]
[104]
Pham, T.H.; Bak, Y.; Kwon, T.; Kwon, S.B.; Oh, J.W.; Park, J.H.; Choi, Y.K.; Hong, J.T.; Yoon, D.Y. Interleukin-32θ inhibits tumor-promoting effects of macrophage-secreted CCL18 in breast cancer. Cell Commun. Signal., 2019, 17(1), 53.
[http://dx.doi.org/10.1186/s12964-019-0374-y] [PMID: 31126309]
[105]
Storr, S.J.; Safuan, S.; Ahmad, N.; El-Refaee, M.; Jackson, A.M.; Martin, S.G. Macrophage-derived interleukin-1beta promotes human breast cancer cell migration and lymphatic adhesion in vitro. Cancer Immunol. Immunother., 2017, 66(10), 1287-1294.
[http://dx.doi.org/10.1007/s00262-017-2020-0] [PMID: 28551814]
[106]
Gillgrass, A.; Gill, N.; Babian, A.; Ashkar, A.A. The absence or overexpression of IL-15 drastically alters breast cancer metastasis via effects on NK cells, CD4 T cells, and macrophages. J. Immunol., 2014, 193(12), 6184-6191.
[http://dx.doi.org/10.4049/jimmunol.1303175] [PMID: 25355926]
[107]
Howe, L.R.; Subbaramaiah, K.; Hudis, C.A.; Dannenberg, A.J. Molecular pathways: Adipose inflammation as a mediator of obesity-associated cancer. Clin. Cancer Res., 2013, 19(22), 6074-6083.
[http://dx.doi.org/10.1158/1078-0432.CCR-12-2603] [PMID: 23958744]
[108]
Li, H.; Yang, B.; Huang, J.; Lin, Y.; Xiang, T.; Wan, J.; Li, H.; Chouaib, S.; Ren, G. Cyclooxygenase-2 in tumor-associated macrophages promotes breast cancer cell survival by triggering a positive-feedback loop between macrophages and cancer cells. Oncotarget, 2015, 6(30), 29637-29650.
[http://dx.doi.org/10.18632/oncotarget.4936] [PMID: 26359357]
[109]
Ma, R.Y.; Zhang, H.; Li, X.F.; Zhang, C.B.; Selli, C.; Tagliavini, G.; Lam, A.D.; Prost, S.; Sims, A.H.; Hu, H.Y.; Ying, T.; Wang, Z.; Ye, Z.; Pollard, J.W.; Qian, B.Z. Monocyte-derived macrophages promote breast cancer bone metastasis outgrowth. J. Exp. Med., 2020, 217(11), e20191820.
[http://dx.doi.org/10.1084/jem.20191820] [PMID: 32780802]
[110]
Valeta-Magara, A.; Gadi, A.; Volta, V.; Walters, B.; Arju, R.; Giashuddin, S.; Zhong, H.; Schneider, R.J. Inflammatory breast cancer promotes development of M2 tumor-associated macrophages and cancer mesenchymal cells through a complex chemokine network. Cancer Res., 2019, 79(13), 3360-3371.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-2158] [PMID: 31043378]
[111]
Al-Jawadi, A.; Moussa, H.; Ramalingam, L.; Dharmawardhane, S.; Gollahon, L.; Gunaratne, P.; Layeequr Rahman, R.; Moustaid-Moussa, N. Protective properties of n-3 fatty acids and implications in obesity-associated breast cancer. J. Nutr. Biochem., 2018, 53, 1-8.
[http://dx.doi.org/10.1016/j.jnutbio.2017.09.018] [PMID: 29096149]
[112]
Cha, Y.J.; Kim, E.S.; Koo, J.S. Tumor-associated macrophages and crown-like structures in adipose tissue in breast cancer. Breast Cancer Res. Treat., 2018, 170(1), 15-25.
[http://dx.doi.org/10.1007/s10549-018-4722-1] [PMID: 29468486]
[113]
Sun, X.; Casbas-Hernandez, P.; Bigelow, C.; Makowski, L.; Joseph Jerry, D.; Smith Schneider, S.; Troester, M.A. Normal breast tissue of obese women is enriched for macrophage markers and macrophage-associated gene expression. Breast Cancer Res. Treat., 2012, 131(3), 1003-1012.
[http://dx.doi.org/10.1007/s10549-011-1789-3] [PMID: 22002519]
[114]
Hao, J.; Yan, F.; Zhang, Y.; Triplett, A.; Zhang, Y.; Schultz, D.A.; Sun, Y.; Zeng, J.; Silverstein, K.A.T.; Zheng, Q.; Bernlohr, D.A.; Cleary, M.P.; Egilmez, N.K.; Sauter, E.; Liu, S.; Suttles, J.; Li, B. Expression of adipocyte/macrophage fatty acid-binding protein in tumor-associated macrophages promotes breast cancer progression. Cancer Res., 2018, 78(9), 2343-2355.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-2465] [PMID: 29437708]
[115]
Gelsomino, L.; Naimo, G.D.; Malivindi, R.; Augimeri, G.; Panza, S.; Giordano, C.; Barone, I.; Bonofiglio, D.; Mauro, L.; Catalano, S.; Andò, S. Knockdown of leptin receptor affects macrophage phenotype in the tumor microenvironment inhibiting breast cancer growth and progression. Cancers (Basel), 2020, 12(8), E2078.
[http://dx.doi.org/10.3390/cancers12082078] [PMID: 32727138]
[116]
Arendt, L.M.; McCready, J.; Keller, P.J.; Baker, D.D.; Naber, S.P.; Seewaldt, V.; Kuperwasser, C. Obesity promotes breast cancer by CCL2-mediated macrophage recruitment and angiogenesis. Cancer Res., 2013, 73(19), 6080-6093.
[http://dx.doi.org/10.1158/0008-5472.CAN-13-0926] [PMID: 23959857]
[117]
Kuziel, G.; Thompson, V.; D’Amato, J.V.; Arendt, L.M. Stromal CCL2 signaling promotes mammary tumor fibrosis through recruitment of myeloid-lineage cells. Cancers (Basel), 2020, 12(8), E2083.
[http://dx.doi.org/10.3390/cancers12082083] [PMID: 32731354]
[118]
Faria, S.S.; Corrêa, L.H.; Heyn, G.S.; de Sant’Ana, L.P.; Almeida, R.D.N.; Magalhães, K.G. Obesity and breast cancer: The role of crown-like structures in breast adipose tissue in tumor progression, prognosis, and therapy. J. Breast Cancer, 2020, 23(3), 233-245.
[http://dx.doi.org/10.4048/jbc.2020.23.e35] [PMID: 32595986]
[119]
Springer, N.L.; Iyengar, N.M.; Bareja, R.; Verma, A.; Jochelson, M.S.; Giri, D.D.; Zhou, X.K.; Elemento, O.; Dannenberg, A.J.; Fischbach, C. Obesity-associated extracellular matrix remodeling promotes a macrophage phenotype similar to tumor-associated macrophages. Am. J. Pathol., 2019, 189(10), 2019-2035.
[http://dx.doi.org/10.1016/j.ajpath.2019.06.005] [PMID: 31323189]
[120]
Lin, L.; Kuhn, C.; Ditsch, N.; Kolben, T.; Czogalla, B.; Beyer, S.; Trillsch, F.; Schmoeckel, E.; Mayr, D.; Mahner, S.; Jeschke, U.; Hester, A. Breast adipose tissue macrophages (BATMs) have a stronger correlation with breast cancer survival than breast tumor stroma macrophages (BTSMs). Breast Cancer Res., 2021, 23(1), 45.
[http://dx.doi.org/10.1186/s13058-021-01422-x] [PMID: 33849622]
[121]
Laforest, S.; Ennour-Idrissi, K.; Ouellette, G.; Gauthier, M.F.; Michaud, A.; Durocher, F.; Tchernof, A.; Diorio, C. Associations between markers of mammary adipose tissue dysfunction and breast cancer prognostic factors. Int. J. Obes., 2021, 45(1), 195-205.
[http://dx.doi.org/10.1038/s41366-020-00676-3] [PMID: 32934318]
[122]
Zeng, J.; Sauter, E.R.; Li, B. FABP4: A new player in obesity-associated breast cancer. Trends Mol. Med., 2020, 26(5), 437-440.
[http://dx.doi.org/10.1016/j.molmed.2020.03.004] [PMID: 32359475]
[123]
Tiwari, P.; Blank, A.; Cui, C.; Schoenfelt, K.Q.; Zhou, G.; Xu, Y.; Khramtsova, G.; Olopade, F.; Shah, A.M.; Khan, S.A.; Rosner, M.R.; Becker, L. Metabolically activated adipose tissue macrophages link obesity to triple-negative breast cancer. J. Exp. Med., 2019, 216(6), 1345-1358.
[http://dx.doi.org/10.1084/jem.20181616] [PMID: 31053611]
[124]
Wagner, M.; Bjerkvig, R.; Wiig, H.; Dudley, A.C. Loss of adipocyte specification and necrosis augment tumor-associated inflammation. Adipocyte, 2013, 2(3), 176-183.
[http://dx.doi.org/10.4161/adip.24472] [PMID: 23991365]
[125]
Jiao, X.; Wang, M.; Zhang, Z.; Li, Z.; Ni, D.; Ashton, A.W.; Tang, H.Y.; Speicher, D.W.; Pestell, R.G. Leronlimab, a humanized monoclonal antibody to CCR5, blocks breast cancer cellular metastasis and enhances cell death induced by DNA damaging chemotherapy. Breast Cancer Res., 2021, 23(1), 11.
[http://dx.doi.org/10.1186/s13058-021-01391-1] [PMID: 33485378]
[126]
Nie, Y.; Huang, H.; Guo, M.; Chen, J.; Wu, W.; Li, W.; Xu, X.; Lin, X.; Fu, W.; Yao, Y.; Zheng, F.; Luo, M.L.; Saw, P.E.; Yao, H.; Song, E.; Hu, H. Breast phyllodes tumors recruit and repolarize tumor-associated macrophages via secreting CCL5 to promote malignant progression, which can be inhibited by CCR5 inhibition therapy. Clin. Cancer Res., 2019, 25(13), 3873-3886.
[http://dx.doi.org/10.1158/1078-0432.CCR-18-3421] [PMID: 30890553]
[127]
Hume, D.A.; MacDonald, K.P. Therapeutic applications of macrophage colony-stimulating factor-1 (CSF-1) and antagonists of CSF-1 receptor (CSF-1R) signaling. Blood, 2012, 119(8), 1810-1820.
[http://dx.doi.org/10.1182/blood-2011-09-379214] [PMID: 22186992]
[128]
Wyckoff, J.B.; Wang, Y.; Lin, E.Y.; Li, J.F.; Goswami, S.; Stanley, E.R.; Segall, J.E.; Pollard, J.W.; Condeelis, J. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res., 2007, 67(6), 2649-2656.
[http://dx.doi.org/10.1158/0008-5472.CAN-06-1823] [PMID: 17363585]
[129]
Fend, L.; Accart, N.; Kintz, J.; Cochin, S.; Reymann, C.; Le Pogam, F.; Marchand, J.B.; Menguy, T.; Slos, P.; Rooke, R.; Fournel, S.; Bonnefoy, J.Y.; Préville, X.; Haegel, H. Therapeutic effects of anti-CD115 monoclonal antibody in mouse cancer models through dual inhibition of tumor-associated macrophages and osteoclasts. PLoS One, 2013, 8(9), e73310.
[http://dx.doi.org/10.1371/journal.pone.0073310] [PMID: 24019914]
[130]
Strachan, D.C.; Ruffell, B.; Oei, Y.; Bissell, M.J.; Coussens, L.M.; Pryer, N.; Daniel, D. 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. OncoImmunology, 2013, 2(12), e26968.
[http://dx.doi.org/10.4161/onci.26968] [PMID: 24498562]
[131]
Ngambenjawong, C.; Gustafson, H.H.; Pun, S.H. Progress in tumor-associated macrophage (TAM)-targeted therapeutics. Adv. Drug Deliv. Rev., 2017, 114, 206-221.
[http://dx.doi.org/10.1016/j.addr.2017.04.010] [PMID: 28449873]
[132]
Lu, X.; Kang, Y. Chemokine (C-C motif) ligand 2 engages CCR2+ stromal cells of monocytic origin to promote breast cancer metastasis to lung and bone. J. Biol. Chem., 2009, 284(42), 29087-29096.
[http://dx.doi.org/10.1074/jbc.M109.035899] [PMID: 19720836]
[133]
Brummer, G.; Fang, W.; Smart, C.; Zinda, B.; Alissa, N.; Berkland, C.; Miller, D.; Cheng, N. CCR2 signaling in breast carcinoma cells promotes tumor growth and invasion by promoting CCL2 and suppressing CD154 effects on the angiogenic and immune microenvironments. Oncogene, 2020, 39(11), 2275-2289.
[http://dx.doi.org/10.1038/s41388-019-1141-7] [PMID: 31827233]
[134]
Yin, S.; Wang, N.; Riabov, V.; Mossel, D.M.; Larionova, I.; Schledzewski, K.; Trofimova, O.; Sevastyanova, T.; Zajakina, A.; Schmuttermaier, C.; Gratchev, A.; Flatley, A.; Kremmer, E.; Zavyalova, M.; Cherdyntseva, N.; Simon-Keller, K.; Marx, A.; Klüter, H.; Goerdt, S.; Kzhyshkowska, J. SI-CLP inhibits the growth of mouse mammary adenocarcinoma by preventing recruitment of tumor-associated macrophages. Int. J. Cancer, 2020, 146(5), 1396-1408.
[http://dx.doi.org/10.1002/ijc.32685] [PMID: 31525266]
[135]
Lim, S.Y.; Yuzhalin, A.E.; Gordon-Weeks, A.N.; Muschel, R.J. Targeting the CCL2-CCR2 signaling axis in cancer metastasis. Oncotarget, 2016, 7(19), 28697-28710.
[http://dx.doi.org/10.18632/oncotarget.7376] [PMID: 26885690]
[136]
Junankar, S.; Shay, G.; Jurczyluk, J.; Ali, N.; Down, J.; Pocock, N.; Parker, A.; Nguyen, A.; Sun, S.; Kashemirov, B.; McKenna, C.E.; Croucher, P.I.; Swarbrick, A.; Weilbaecher, K.; Phan, T.G.; Rogers, M.J. Real-time intravital imaging establishes tumor-associated macrophages as the extraskeletal target of bisphosphonate action in cancer. Cancer Discov., 2015, 5(1), 35-42.
[http://dx.doi.org/10.1158/2159-8290.CD-14-0621] [PMID: 25312016]
[137]
Rogers, T.L.; Holen, I. Tumour macrophages as potential targets of bisphosphonates. J. Transl. Med., 2011, 9(1), 177.
[http://dx.doi.org/10.1186/1479-5876-9-177] [PMID: 22005011]
[138]
Pang, Y.; Fu, Y.; Li, C.; Wu, Z.; Cao, W.; Hu, X.; Sun, X.; He, W.; Cao, X.; Ling, D.; Li, Q.; Fan, C.; Yang, C.; Kong, X.; Qin, A. Metal-organic framework nanoparticles for ameliorating breast cancer-associated osteolysis. Nano Lett., 2020, 20(2), 829-840.
[http://dx.doi.org/10.1021/acs.nanolett.9b02916] [PMID: 31916446]
[139]
Pallardy, M.J.; Turbica, I.; Biola-Vidamment, A. Why the immune system should be concerned by nanomaterials? Front. Immunol., 2017, 8, 544.
[http://dx.doi.org/10.3389/fimmu.2017.00544] [PMID: 28555135]
[140]
Li, S.; Wu, Y.; Ding, F.; Yang, J.; Li, J.; Gao, X.; Zhang, C.; Feng, J. Engineering macrophage-derived exosomes for targeted chemotherapy of triple-negative breast cancer. Nanoscale, 2020, 12(19), 10854-10862.
[http://dx.doi.org/10.1039/D0NR00523A] [PMID: 32396590]
[141]
Haney, M.J.; Zhao, Y.; Jin, Y.S.; Li, S.M.; Bago, J.R.; Klyachko, N.L.; Kabanov, A.V.; Batrakova, E.V. Macrophage-derived extracellular vesicles as drug delivery systems for triple negative breast cancer (TNBC) therapy. J. Neuroimmune Pharmacol., 2020, 15(3), 487-500.
[http://dx.doi.org/10.1007/s11481-019-09884-9] [PMID: 31722094]
[142]
Liu, L.; Lu, Y.; Martinez, J.; Bi, Y.; Lian, G.; Wang, T.; Milasta, S.; Wang, J.; Yang, M.; Liu, G.; Green, D.R.; Wang, R. Proinflammatory signal suppresses proliferation and shifts macrophage metabolism from Myc-dependent to HIF1α-dependent. Proc. Natl. Acad. Sci. USA, 2016, 113(6), 1564-1569.
[http://dx.doi.org/10.1073/pnas.1518000113] [PMID: 26811453]
[143]
Esser, A.K.; Ross, M.H.; Fontana, F.; Su, X.; Gabay, A.; Fox, G.C.; Xu, Y.; Xiang, J.; Schmieder, A.H.; Yang, X.; Cui, G.; Scott, M.; Achilefu, S.; Chauhan, J.; Fletcher, S.; Lanza, G.M.; Weilbaecher, K.N. Nanotherapy delivery of c-myc inhibitor targets protumor macrophages and preserves antitumor macrophages in breast cancer. Theranostics, 2020, 10(17), 7510-7526.
[http://dx.doi.org/10.7150/thno.44523] [PMID: 32685002]
[144]
Obeid, E.; Nanda, R.; Fu, Y.X.; Olopade, O.I. The role of tumor-associated macrophages in breast cancer progression (review). Int. J. Oncol., 2013, 43(1), 5-12.
[http://dx.doi.org/10.3892/ijo.2013.1938] [PMID: 23673510]
[145]
Cassetta, L.; Pollard, J.W. Targeting macrophages: Therapeutic approaches in cancer. Nat. Rev. Drug Discov., 2018, 17(12), 887-904.
[http://dx.doi.org/10.1038/nrd.2018.169] [PMID: 30361552]
[146]
Sureshchandra, S.; Wilson, R.M.; Rais, M.; Marshall, N.E.; Purnell, J.Q.; Thornburg, K.L.; Messaoudi, I. Maternal pregravid obesity remodels the DNA methylation landscape of cord blood monocytes disrupting their inflammatory program. J. Immunol., 2017, 199(8), 2729-2744.
[http://dx.doi.org/10.4049/jimmunol.1700434] [PMID: 28887432]
[147]
Wyckoff, J.; Wang, W.; Lin, E.Y.; Wang, Y.; Pixley, F.; Stanley, E.R.; Graf, T.; Pollard, J.W.; Segall, J.; Condeelis, J. A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res., 2004, 64(19), 7022-7029.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-1449] [PMID: 15466195]
[148]
Fang, W.; Zhou, T.; Shi, H.; Yao, M.; Zhang, D.; Qian, H.; Zeng, Q.; Wang, Y.; Jin, F.; Chai, C.; Chen, T. Progranulin induces immune escape in breast cancer via up-regulating PD-L1 expression on tumor-associated macrophages (TAMs) and promoting CD8+ T cell exclusion. J. Exp. Clin. Cancer Res., 2021, 40(1), 4.
[http://dx.doi.org/10.1186/s13046-020-01786-6] [PMID: 33390170]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy