Crosstalk Between Macrophages and Breast Cancer Cells: Networking Within Tumors.
Breast cancer
Intercellular communication
Metastasis
Tumor associated macrophages
Tumor microenvironment
Tunneling nanotubes
Journal
Results and problems in cell differentiation
ISSN: 0080-1844
Titre abrégé: Results Probl Cell Differ
Pays: Germany
ID NLM: 0173555
Informations de publication
Date de publication:
2024
2024
Historique:
medline:
16
10
2024
pubmed:
16
10
2024
entrez:
15
10
2024
Statut:
ppublish
Résumé
Tumor associated macrophages (TAMs) are one of the most prominent immune cells in the breast tumor microenvironment (TME). TAMs are categorised into classically activated anti-tumorigenic M1 and alternatively activated pro-tumorigenic M2 macrophages. TAMs are known to promote cancer pathogenesis by facilitating cancer cell and cancer stem cell growth, angiogenesis, immune evasion, invasion, and migration. Consequently, TAMs drive cancer progression towards metastasis. This chapter describes the role of TME in driving monocyte recruitment and polarization toward the M2 phenotype. We also illustrate the modalities of intercellular networking such as paracrine signaling, exosomes, and tunneling nanotubes (TNTs) that TAMs and cancer cells employ within TME to communicate with each other and with other cells of TME to facilitate the dynamic process of cancer progression. Finally, we discuss the clinical implications of TAMs in breast cancer and potential therapeutic strategies targeting TAM recruitment, polarization, and TAM-mediated immune evasion for effective cancer therapy.
Identifiants
pubmed: 39406907
doi: 10.1007/978-3-031-65944-7_8
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
213-238Informations de copyright
© 2024. The Author(s), under exclusive license to Springer Nature Switzerland AG.
Références
Abraham D et al (2010) Stromal cell-derived CSF-1 blockade prolongs xenograft survival of CSF-1-negative neuroblastoma. Int J Cancer 126(6):1339–1352
doi: 10.1002/ijc.24859
Allavena P et al (2005) Anti-inflammatory properties of the novel antitumor agent yondelis (trabectedin): inhibition of macrophage differentiation and cytokine production. Cancer Res 65(7):2964–2971
doi: 10.1158/0008-5472.CAN-04-4037
Allavena P, Digifico E, Belgiovine C (2021) Macrophages and cancer stem cells: a malevolent alliance. Mol Med 27(1):121
doi: 10.1186/s10020-021-00383-3
Allison E et al (2023) Breast cancer survival outcomes and tumor-associated macrophage markers: a systematic review and meta-analysis. Oncol Ther 11(1):27–48
doi: 10.1007/s40487-022-00214-3
Amintas S et al (2020) Circulating tumor cell clusters: united we stand divided we fall. Int J Mol Sci 21(7)
An G et al (2019) Effects of CCL5 on the biological behavior of breast cancer and the mechanisms of its interaction with tumor-associated macrophages. Oncol Rep 42(6):2499–2511
Aras S, Zaidi MR (2017) TAMeless traitors: macrophages in cancer progression and metastasis. Br J Cancer 117(11):1583–1591
doi: 10.1038/bjc.2017.356
Baeriswyl V, Christofori G (2009) The angiogenic switch in carcinogenesis. Semin Cancer Biol 19(5):329–337
doi: 10.1016/j.semcancer.2009.05.003
Bergers G, Benjamin LE (2003) Tumorigenesis and the angiogenic switch. Nat Rev Cancer 3(6):401–410
doi: 10.1038/nrc1093
Bertolini I et al (2019) A GBM-like V-ATPase signature directs cell-cell tumor signaling and reprogramming via large oncosomes. EBioMedicine 41:225–235
doi: 10.1016/j.ebiom.2019.01.051
Bronte V et al (2016) Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards. Nat Commun 7:12150
doi: 10.1038/ncomms12150
Cao R et al (2015) Collaborative effects between the TNFα-TNFR1-macrophage axis and the VEGF-C-VEGFR3 signaling in lymphangiogenesis and metastasis. Oncoimmunology 4(3):e989777
doi: 10.4161/2162402X.2014.989777
Carter KP et al (2019) Macrophages enhance 3D invasion in a breast cancer cell line by induction of tumor cell tunneling nanotubes. Cancer Rep (Hoboken) 2(6):e1213
doi: 10.1002/cnr2.1213
Chen Q, Zhang XH, Massagué J (2011a) Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Cancer Cell 20(4):538–549
doi: 10.1016/j.ccr.2011.08.025
Chen J et al (2011b) CCL18 from tumor-associated macrophages promotes breast cancer metastasis via PITPNM3. Cancer Cell 19(4):541–555
doi: 10.1016/j.ccr.2011.02.006
Chen Y et al (2017) Tumor-recruited M2 macrophages promote gastric and breast cancer metastasis via M2 macrophage-secreted CHI3L1 protein. J Hematol Oncol 10(1):36
doi: 10.1186/s13045-017-0408-0
Chen X et al (2022) Tumor-associated macrophages promote epithelial-mesenchymal transition and the cancer stem cell properties in triple-negative breast cancer through CCL2/AKT/β-catenin signaling. Cell Commun Signal 20(1):92
doi: 10.1186/s12964-022-00888-2
Chuo ST, Chien JC, Lai CP (2018) Imaging extracellular vesicles: current and emerging methods. J Biomed Sci 25(1):91
doi: 10.1186/s12929-018-0494-5
Condeelis J, Pollard JW (2006) Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124(2):263–266
doi: 10.1016/j.cell.2006.01.007
Condeelis J, Segall JE (2003) Intravital imaging of cell movement in tumours. Nat Rev Cancer 3(12):921–930
doi: 10.1038/nrc1231
Dallavalasa S et al (2021) The role of tumor associated macrophages (TAMs) in cancer progression, chemoresistance, angiogenesis and metastasis - current status. Curr Med Chem 28(39):8203–8236
doi: 10.2174/0929867328666210720143721
de Boniface J et al (2012) Expression patterns of the immunomodulatory enzyme arginase 1 in blood, lymph nodes and tumor tissue of early-stage breast cancer patients. Oncoimmunology 1(8):1305–1312
doi: 10.4161/onci.21678
Di Vizio D et al (2009) Oncosome formation in prostate cancer: association with a region of frequent chromosomal deletion in metastatic disease. Cancer Res 69(13):5601–5609
doi: 10.1158/0008-5472.CAN-08-3860
Di Vizio D et al (2012) Large oncosomes in human prostate cancer tissues and in the circulation of mice with metastatic disease. Am J Pathol 181(5):1573–1584
doi: 10.1016/j.ajpath.2012.07.030
Dunn GP, Old LJ, Schreiber RD (2004) The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21(2):137–148
doi: 10.1016/j.immuni.2004.07.017
Dvorak HF (1986) Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 315(26):1650–1659
doi: 10.1056/NEJM198612253152606
Edin S et al (2013) Macrophages: good guys in colorectal cancer. Oncoimmunology 2(2):e23038
doi: 10.4161/onci.23038
Fang HY et al (2009) Hypoxia-inducible factors 1 and 2 are important transcriptional effectors in primary macrophages experiencing hypoxia. Blood 114(4):844–859
doi: 10.1182/blood-2008-12-195941
Farhood B, Najafi M, Mortezaee K (2019) CD8(+) cytotoxic T lymphocytes in cancer immunotherapy: a review. J Cell Physiol 234(6):8509–8521
doi: 10.1002/jcp.27782
Farzaneh Behelgardi M et al (2020) Targeting signaling pathways of VEGFR1 and VEGFR2 as a potential target in the treatment of breast cancer. Mol Biol Rep 47(3):2061–2071
doi: 10.1007/s11033-020-05306-9
Ferlay J et al (2021) Cancer statistics for the year 2020: an overview. Int J Cancer
Franklin RA et al (2014) The cellular and molecular origin of tumor-associated macrophages. Science 344(6186):921–925
doi: 10.1126/science.1252510
Fu XT et al (2015) Macrophage-secreted IL-8 induces epithelial-mesenchymal transition in hepatocellular carcinoma cells by activating the JAK2/STAT3/Snail pathway. Int J Oncol 46(2):587–596
doi: 10.3892/ijo.2014.2761
Fu LQ et al (2020) The roles of tumor-associated macrophages in tumor angiogenesis and metastasis. Cell Immunol 353:104119
doi: 10.1016/j.cellimm.2020.104119
Gazzaniga S et al (2007) Targeting tumor-associated macrophages and inhibition of MCP-1 reduce angiogenesis and tumor growth in a human melanoma xenograft. J Invest Dermatol 127(8):2031–2041
doi: 10.1038/sj.jid.5700827
Geiger TR, Peeper DS (2009) Metastasis mechanisms. Biochim Biophys Acta 1796(2):293–308
Genard G, Lucas S, Michiels C (2017) Reprogramming of tumor-associated macrophages with anticancer therapies: radiotherapy versus chemo- and immunotherapies. Front Immunol 8:828
doi: 10.3389/fimmu.2017.00828
Giatromanolaki A et al (2006) Hypoxia-inducible factor-2 alpha (HIF-2 alpha) induces angiogenesis in breast carcinomas. Appl Immunohistochem Mol Morphol 14(1):78–82
doi: 10.1097/01.pai.0000145182.98577.10
Gil-Bernabé AM et al (2012) Recruitment of monocytes/macrophages by tissue factor-mediated coagulation is essential for metastatic cell survival and premetastatic niche establishment in mice. Blood 119(13):3164–3175
doi: 10.1182/blood-2011-08-376426
Gocheva V et al (2010) IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion. Genes Dev 24(3):241–255
doi: 10.1101/gad.1874010
Goede V et al (1999) Induction of inflammatory angiogenesis by monocyte chemoattractant protein-1. Int J Cancer 82(5):765–770
doi: 10.1002/(SICI)1097-0215(19990827)82:5<765::AID-IJC23>3.0.CO;2-F
Gordon SR et al (2017) PD-1 expression by tumour-associated macrophages inhibits phagocytosis and tumour immunity. Nature 545(7655):495–499
doi: 10.1038/nature22396
György B et al (2011) Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci 68(16):2667–2688
doi: 10.1007/s00018-011-0689-3
Hambardzumyan D, Gutmann DH, Kettenmann H (2016) The role of microglia and macrophages in glioma maintenance and progression. Nat Neurosci 19(1):20–27
doi: 10.1038/nn.4185
Han L, Lam EW, Sun Y (2019) Extracellular vesicles in the tumor microenvironment: old stories, but new tales. Mol Cancer 18(1):59
doi: 10.1186/s12943-019-0980-8
Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100(1):57–70
doi: 10.1016/S0092-8674(00)81683-9
Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646–674
doi: 10.1016/j.cell.2011.02.013
Hanna SJ et al (2019) Tunneling nanotubes, a novel mode of tumor cell-macrophage communication in tumor cell invasion. J Cell Sci 132(3)
Hao NB et al (2012) Macrophages in tumor microenvironments and the progression of tumors. Clin Dev Immunol 2012:948098
doi: 10.1155/2012/948098
Headley MB et al (2016) Visualization of immediate immune responses to pioneer metastatic cells in the lung. Nature 531(7595):513–517
doi: 10.1038/nature16985
Hossain MA et al (2021) Reinvigorating exhausted CD8(+) cytotoxic T lymphocytes in the tumor microenvironment and current strategies in cancer immunotherapy. Med Res Rev 41(1):156–201
doi: 10.1002/med.21727
Hume DA, MacDonald KP (2012) Therapeutic applications of macrophage colony-stimulating factor-1 (CSF-1) and antagonists of CSF-1 receptor (CSF-1R) signaling. Blood 119(8):1810–1820
doi: 10.1182/blood-2011-09-379214
Hwang I et al (2020) Tumor-associated macrophage, angiogenesis and lymphangiogenesis markers predict prognosis of non-small cell lung cancer patients. J Transl Med 18(1):443
doi: 10.1186/s12967-020-02618-z
Jia X et al (2014) Emodin suppresses pulmonary metastasis of breast cancer accompanied with decreased macrophage recruitment and M2 polarization in the lungs. Breast Cancer Res Treat 148(2):291–302
doi: 10.1007/s10549-014-3164-7
Kaplan RN et al (2005) VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438(7069):820–827
doi: 10.1038/nature04186
Kaplan RN, Psaila B, Lyden D (2006) Bone marrow cells in the ‘pre-metastatic niche’: within bone and beyond. Cancer Metastasis Rev 25(4):521–529
doi: 10.1007/s10555-006-9036-9
Kessenbrock K, Plaks V, Werb Z (2010) Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141(1):52–67
doi: 10.1016/j.cell.2010.03.015
Krausgruber T et al (2011) IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat Immunol 12(3):231–238
doi: 10.1038/ni.1990
Kumar V et al (2016) The nature of myeloid-derived suppressor cells in the tumor microenvironment. Trends Immunol 37(3):208–220
doi: 10.1016/j.it.2016.01.004
LaGory EL, Giaccia AJ (2016) The ever-expanding role of HIF in tumour and stromal biology. Nat Cell Biol 18(4):356–365
doi: 10.1038/ncb3330
Lee AH et al (1997) Angiogenesis and inflammation in invasive carcinoma of the breast. J Clin Pathol 50(8):669–673
doi: 10.1136/jcp.50.8.669
Lee HD et al (2012) Exosome release of ADAM15 and the functional implications of human macrophage-derived ADAM15 exosomes. FASEB J 26(7):3084–3095
doi: 10.1096/fj.11-201681
Lee CW et al (2022) Effects of the media conditioned by various macrophage subtypes derived from THP-1 cells on tunneling nanotube formation in pancreatic cancer cells. BMC Mol Cell Biol 23(1):26
doi: 10.1186/s12860-022-00428-3
Leek RD et al (1996) Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res 56(20):4625–4629
Li J et al (2020a) Tumor-associated macrophage infiltration and prognosis in colorectal cancer: systematic review and meta-analysis. Int J Colorectal Dis 35(7):1203–1210
doi: 10.1007/s00384-020-03593-z
Li D et al (2020b) Tumor-associated macrophages secrete CC-chemokine ligand 2 and induce tamoxifen resistance by activating PI3K/Akt/mTOR in breast cancer. Cancer Sci 111(1):47–58
doi: 10.1111/cas.14230
Li J et al (2023) A comprehensive review on the composition, biogenesis, purification, and multifunctional role of exosome as delivery vehicles for cancer therapy. Biomed Pharmacother 165:115087
doi: 10.1016/j.biopha.2023.115087
Lin EY et al (2006) Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Cancer Res 66(23):11238–11246
doi: 10.1158/0008-5472.CAN-06-1278
Lin Y, Xu J, Lan H (2019) Tumor-associated macrophages in tumor metastasis: biological roles and clinical therapeutic applications. J Hematol Oncol 12(1):76
doi: 10.1186/s13045-019-0760-3
Linde N et al (2012) Vascular endothelial growth factor-induced skin carcinogenesis depends on recruitment and alternative activation of macrophages. J Pathol 227(1):17–28
doi: 10.1002/path.3989
Liou GY, Storz P (2010) Reactive oxygen species in cancer. Free Radic Res 44(5):479–496
doi: 10.3109/10715761003667554
Lu X, Kang Y (2007) Organotropism of breast cancer metastasis. J Mammary Gland Biol Neoplasia 12(2-3):153–162
doi: 10.1007/s10911-007-9047-3
Lu X, Kang Y (2009) 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 284(42):29087–29096
doi: 10.1074/jbc.M109.035899
Lu X et al (2011) VCAM-1 promotes osteolytic expansion of indolent bone micrometastasis of breast cancer by engaging α4β1-positive osteoclast progenitors. Cancer Cell 20(6):701–714
doi: 10.1016/j.ccr.2011.11.002
Mahmoud SM et al (2012) Tumour-infiltrating macrophages and clinical outcome in breast cancer. J Clin Pathol 65(2):159–163
doi: 10.1136/jclinpath-2011-200355
Mantovani A et al (2002) Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 23(11):549–555
doi: 10.1016/S1471-4906(02)02302-5
Mantovani A et al (2008) Cancer-related inflammation. Nature 454(7203):436–444
doi: 10.1038/nature07205
Mantovani A et al (2017) Tumour-associated macrophages as treatment targets in oncology. Nat Rev Clin Oncol 14(7):399–416
doi: 10.1038/nrclinonc.2016.217
Melwani PK, Pandey BN (2023) Tunneling nanotubes: the intercellular conduits contributing to cancer pathogenesis and its therapy. Biochim Biophys Acta Rev Cancer 1878(6):189028
doi: 10.1016/j.bbcan.2023.189028
Melwani PK et al (2021) Integrated transcriptomic and proteomic analysis of microplasts derived from macrophage-conditioned medium-treated MCF-7 breast cancer cells. FEBS Lett 595(13):1844–1860
doi: 10.1002/1873-3468.14108
Minciacchi VR, Freeman MR, Di Vizio D (2015) Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes. Semin Cell Dev Biol 40:41–51
doi: 10.1016/j.semcdb.2015.02.010
Mizutani K et al (2009) The chemokine CCL2 increases prostate tumor growth and bone metastasis through macrophage and osteoclast recruitment. Neoplasia 11(11):1235–1242
doi: 10.1593/neo.09988
Morrissey SM et al (2021) Tumor-derived exosomes drive immunosuppressive macrophages in a pre-metastatic niche through glycolytic dominant metabolic reprogramming. Cell Metab 33(10):2040–2058.e10
doi: 10.1016/j.cmet.2021.09.002
Mougiakakos D et al (2010) Regulatory T cells in cancer. Adv Cancer Res 107:57–117
doi: 10.1016/S0065-230X(10)07003-X
Movahedi K et al (2010) Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res 70(14):5728–5739
doi: 10.1158/0008-5472.CAN-09-4672
Müller A et al (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410(6824):50–56
doi: 10.1038/35065016
Munder M (2009) Arginase: an emerging key player in the mammalian immune system. Br J Pharmacol 158(3):638–651
doi: 10.1111/j.1476-5381.2009.00291.x
Murdoch C et al (2007) Expression of Tie-2 by human monocytes and their responses to angiopoietin-2. J Immunol 178(11):7405–7411
doi: 10.4049/jimmunol.178.11.7405
Murray PJ et al (2014) Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 41(1):14–20
doi: 10.1016/j.immuni.2014.06.008
Netea-Maier RT, Smit JWA, Netea MG (2018) Metabolic changes in tumor cells and tumor-associated macrophages: a mutual relationship. Cancer Lett 413:102–109
doi: 10.1016/j.canlet.2017.10.037
Nie Y et al (2019) 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 25(13):3873–3886
doi: 10.1158/1078-0432.CCR-18-3421
Nie X et al (2023) Garcinone E suppresses breast cancer growth and metastasis by modulating tumor-associated macrophages polarization via STAT6 signaling. Phytother Res 37(10):4442–4456
doi: 10.1002/ptr.7909
Nierodzik ML, Karpatkin S (2006) Thrombin induces tumor growth, metastasis, and angiogenesis: evidence for a thrombin-regulated dormant tumor phenotype. Cancer Cell 10(5):355–362
doi: 10.1016/j.ccr.2006.10.002
Noy R, Pollard JW (2014) Tumor-associated macrophages: from mechanisms to therapy. Immunity 41(1):49–61
doi: 10.1016/j.immuni.2014.06.010
Okabe Y, Medzhitov R (2014) Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 157(4):832–844
doi: 10.1016/j.cell.2014.04.016
Onfelt B et al (2006) Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria. J Immunol 177(12):8476–8483
doi: 10.4049/jimmunol.177.12.8476
Osswald M et al (2015) Brain tumour cells interconnect to a functional and resistant network. Nature 528(7580):93–98
doi: 10.1038/nature16071
Ostrand-Rosenberg S, Sinha P (2009) Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 182(8):4499–4506
doi: 10.4049/jimmunol.0802740
Otsuji M et al (1996) Oxidative stress by tumor-derived macrophages suppresses the expression of CD3 zeta chain of T-cell receptor complex and antigen-specific T-cell responses. Proc Natl Acad Sci U S A 93(23):13119–13124
doi: 10.1073/pnas.93.23.13119
Palumbo JS et al (2007) Tumor cell-associated tissue factor and circulating hemostatic factors cooperate to increase metastatic potential through natural killer cell-dependent and-independent mechanisms. Blood 110(1):133–141
doi: 10.1182/blood-2007-01-065995
Pan Y et al (2020) Tumor-associated macrophages in tumor immunity. Front Immunol 11:583084
doi: 10.3389/fimmu.2020.583084
Patheja P, Sahu K (2017) Macrophage conditioned medium induced cellular network formation in MCF-7 cells through enhanced tunneling nanotube formation and tunneling nanotube mediated release of viable cytoplasmic fragments. Exp Cell Res 355(2):182–193
doi: 10.1016/j.yexcr.2017.04.008
Pinto G, Brou C, Zurzolo C (2020) Tunneling nanotubes: the fuel of tumor progression? Trends Cancer 6(10):874–888
doi: 10.1016/j.trecan.2020.04.012
Pollard JW (2004) Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 4(1):71–78
doi: 10.1038/nrc1256
Qian BZ, Pollard JW (2010) Macrophage diversity enhances tumor progression and metastasis. Cell 141(1):39–51
doi: 10.1016/j.cell.2010.03.014
Qian B et al (2009) A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS One 4(8):e6562
doi: 10.1371/journal.pone.0006562
Qian BZ et al (2011) CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 475(7355):222–225
doi: 10.1038/nature10138
Racioppi L et al (2019) CaMKK2 in myeloid cells is a key regulator of the immune-suppressive microenvironment in breast cancer. Nat Commun 10(1):2450
doi: 10.1038/s41467-019-10424-5
Ramesh A et al (2019) CSF1R- and SHP2-inhibitor-loaded nanoparticles enhance cytotoxic activity and phagocytosis in tumor-associated macrophages. Adv Mater 31(51):e1904364
doi: 10.1002/adma.201904364
Ravi J et al (2016) Cannabinoid receptor-2 agonist inhibits macrophage induced EMT in non-small cell lung cancer by downregulation of EGFR pathway. Mol Carcinog 55(12):2063–2076
doi: 10.1002/mc.22451
Riabov V et al (2014) Role of tumor associated macrophages in tumor angiogenesis and lymphangiogenesis. Front Physiol 5:75
doi: 10.3389/fphys.2014.00075
Rihawi K et al (2021) Tumor-associated macrophages and inflammatory microenvironment in gastric cancer: novel translational implications. Int J Mol Sci 22(8)
Robinson BD et al (2009) Tumor microenvironment of metastasis in human breast carcinoma: a potential prognostic marker linked to hematogenous dissemination. Clin Cancer Res 15(7):2433–2441
doi: 10.1158/1078-0432.CCR-08-2179
Roehlecke C, Schmidt MHH (2020) Tunneling nanotubes and tumor microtubes in cancer. Cancers (Basel) 12(4)
Rolny C et al (2011) HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell 19(1):31–44
doi: 10.1016/j.ccr.2010.11.009
Rustom A et al (2004) Nanotubular highways for intercellular organelle transport. Science 303(5660):1007–1010
doi: 10.1126/science.1093133
Saji H et al (2001) Significant correlation of monocyte chemoattractant protein-1 expression with neovascularization and progression of breast carcinoma. Cancer 92(5):1085–1091
doi: 10.1002/1097-0142(20010901)92:5<1085::AID-CNCR1424>3.0.CO;2-K
Sangaletti S et al (2008) Macrophage-derived SPARC bridges tumor cell-extracellular matrix interactions toward metastasis. Cancer Res 68(21):9050–9059
doi: 10.1158/0008-5472.CAN-08-1327
Sceneay J, Smyth MJ, Möller A (2013) The pre-metastatic niche: finding common ground. Cancer Metastasis Rev 32(3–4):449–464
doi: 10.1007/s10555-013-9420-1
Schäfer M, Werner S (2008) Cancer as an overhealing wound: an old hypothesis revisited. Nat Rev Mol Cell Biol 9(8):628–638
doi: 10.1038/nrm2455
Shields JD et al (2010) Induction of lymphoidlike stroma and immune escape by tumors that express the chemokine CCL21. Science 328(5979):749–752
doi: 10.1126/science.1185837
Sierra-Filardi E et al (2014) CCL2 shapes macrophage polarization by GM-CSF and M-CSF: identification of CCL2/CCR2-dependent gene expression profile. J Immunol 192(8):3858–3867
doi: 10.4049/jimmunol.1302821
Strachan DC et al (2013) CSF1R inhibition delays cervical and mammary tumor growth in murine models by attenuating the turnover of tumor-associated macrophages and enhancing infiltration by CD8. Oncoimmunology 2(12):e26968
doi: 10.4161/onci.26968
Su S et al (2014) A positive feedback loop between mesenchymal-like cancer cells and macrophages is essential to breast cancer metastasis. Cancer Cell 25(5):605–620
doi: 10.1016/j.ccr.2014.03.021
Su T et al (2021) Exosomal MicroRNAs mediating crosstalk between cancer cells with cancer-associated fibroblasts and tumor-associated macrophages in the tumor microenvironment. Front Oncol 11:631703
doi: 10.3389/fonc.2021.631703
Tamura R et al (2019) The role of vascular endothelial growth factor in the hypoxic and immunosuppressive tumor microenvironment: perspectives for therapeutic implications. Med Oncol 37(1):2
doi: 10.1007/s12032-019-1329-2
Torroella-Kouri M et al (2005) Diminished expression of transcription factors nuclear factor kappaB and CCAAT/enhancer binding protein underlies a novel tumor evasion mechanism affecting macrophages of mammary tumor-bearing mice. Cancer Res 65(22):10578–10584
doi: 10.1158/0008-5472.CAN-05-0365
Tsutsui S et al (2005) Macrophage infiltration and its prognostic implications in breast cancer: the relationship with VEGF expression and microvessel density. Oncol Rep 14(2):425–431
Ueno T et al (2000) Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer. Clin Cancer Res 6(8):3282–3289
Ugel S et al (2015) Tumor-induced myeloid deviation: when myeloid-derived suppressor cells meet tumor-associated macrophages. J Clin Invest 125(9):3365–3376
doi: 10.1172/JCI80006
Vader P, Breakefield XO, Wood MJ (2014) Extracellular vesicles: emerging targets for cancer therapy. Trends Mol Med 20(7):385–393
doi: 10.1016/j.molmed.2014.03.002
Valković T et al (2002) Correlation between vascular endothelial growth factor, angiogenesis, and tumor-associated macrophages in invasive ductal breast carcinoma. Virchows Arch 440(6):583–588
doi: 10.1007/s004280100458
Vasiljeva O et al (2006) Tumor cell-derived and macrophage-derived cathepsin B promotes progression and lung metastasis of mammary cancer. Cancer Res 66(10):5242–5250
doi: 10.1158/0008-5472.CAN-05-4463
Venneri MA et al (2007) Identification of proangiogenic TIE2-expressing monocytes (TEMs) in human peripheral blood and cancer. Blood 109(12):5276–5285
doi: 10.1182/blood-2006-10-053504
Volodko N et al (1998) Tumour-associated macrophages in breast cancer and their prognostic correlations. The Breast 7(2):99–105
doi: 10.1016/S0960-9776(98)90065-0
Wanderley CW et al (2018) Paclitaxel reduces tumor growth by reprogramming tumor-associated macrophages to an M1 profile in a TLR4-dependent manner. Cancer Res 78(20):5891–5900
doi: 10.1158/0008-5472.CAN-17-3480
Wang P et al (2019) Exosomes from M1-polarized macrophages enhance paclitaxel antitumor activity by activating macrophages-mediated inflammation. Theranostics 9(6):1714–1727
doi: 10.7150/thno.30716
Wu P et al (2016) Inverse role of distinct subsets and distribution of macrophage in lung cancer prognosis: a meta-analysis. Oncotarget 7(26):40451–40460
doi: 10.18632/oncotarget.9625
Wyckoff J et al (2004) A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res 64(19):7022–7029
doi: 10.1158/0008-5472.CAN-04-1449
Wynn TA, Chawla A, Pollard JW (2013) Macrophage biology in development, homeostasis and disease. Nature 496(7446):445–455
doi: 10.1038/nature12034
Xiao H et al (2020) M2-like tumor-associated macrophage-targeted codelivery of STAT6 inhibitor and IKKβ siRNA induces M2-to-M1 repolarization for cancer immunotherapy with low immune side effects. ACS Cent Sci 6(7):1208–1222
doi: 10.1021/acscentsci.9b01235
Yang L, Pang Y, Moses HL (2010) TGF-beta and immune cells: an important regulatory axis in the tumor microenvironment and progression. Trends Immunol 31(6):220–227
doi: 10.1016/j.it.2010.04.002
Yang M et al (2011) Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer 10:117
doi: 10.1186/1476-4598-10-117
Yin S et al (2017) The prognostic and clinicopathological significance of tumor-associated macrophages in patients with gastric cancer: a meta-analysis. PLoS One 12(1):e0170042
doi: 10.1371/journal.pone.0170042
Yount G et al (2007) Independent motile microplast formation correlates with glioma cell invasiveness. J Neurooncol 81(2):113–121
doi: 10.1007/s11060-006-9211-4
Yu X et al (2019) Exosomes from macrophages exposed to apoptotic breast cancer cells promote breast cancer proliferation and metastasis. J Cancer 10(13):2892–2906
doi: 10.7150/jca.31241
Yue S et al (2021) PGRN. Life Sci 264:118687
doi: 10.1016/j.lfs.2020.118687
Zhang J et al (2015) Regulation of epithelial-mesenchymal transition by tumor-associated macrophages in cancer. Am J Transl Res 7(10):1699–1711
Zhang J et al (2016) High infiltration of tumor-associated macrophages influences poor prognosis in human gastric cancer patients, associates with the phenomenon of EMT. Medicine (Baltimore) 95(6):e2636
doi: 10.1097/MD.0000000000002636
Zhao X et al (2017) Prognostic significance of tumor-associated macrophages in breast cancer: a meta-analysis of the literature. Oncotarget 8(18):30576–30586
doi: 10.18632/oncotarget.15736
Zhou J et al (2020) Tumor-associated macrophages: recent insights and therapies. Front Oncol 10:188
doi: 10.3389/fonc.2020.00188
Ziech D et al (2011) Reactive oxygen species (ROS)--induced genetic and epigenetic alterations in human carcinogenesis. Mutat Res 711(1–2):167–173
doi: 10.1016/j.mrfmmm.2011.02.015