Host microenvironment in breast cancer development: Inflammatory and immune cells in tumour angiogenesis and arteriogenesis
Open accessAbstract
Breast cancer progression is associated with and dependent upon robust neovascularization. It is becoming clear that tumour-associated 'normal' cells, such as immune/inflammatory cells, endothelial cells and stromal cells, conspire with cancer cells in promoting this process. In particular, infiltrating immune/inflammatory cells secrete a diverse repertoire of growth factors and proteases that enable them to enhance tumour growth by stimulating angiogenesis and, as we suggest here, by promoting 'tumour arteriogenesis' - enlargement of feeding vessels supplying the expanding tumour capillary bed. Macrophages and their chemoattractants (e.g. macrophage chemoattractant protein-1) are critical for the arteriogenic process in ischaemia, and probably also in breast neoplasia. A better understanding of these various cellular and molecular constituents of breast cancer neovascularization may be useful in designing more effective therapies.
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The appearance of tumor-supporting, iron-donating immune cells, in particular macrophages, is associated with tumor size and aggressiveness as well as poor patient prognosis.
“Of note, the appearance of tumor-supporting, iron-donating immune cells, in particular macrophages, is associated with tumor size and aggressiveness as well as poor patient prognosis [56,57].”
From Iron as a central player and promising target in cancer progression (2019) · cites this paper as [57]
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“possess both direct and indirect tumouricidal activity [5,6].”
BackgroundXu, Y., Hagège, J., Doublet, J.-D., Callard, P., Sraer, J., Rønne, E., & Rondeau, É. (1997) · Human Pathology · doi:10.1016/s0046-8177(97)90108-8 · Cited by 26 · see citing works
Valković, T., Dobrila, F., Melato, M., Sasso, F., Rizzardi, C., & Jonjić, N. (2002) · Cited by 24 · see citing works
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Flagged first, then by citations
Cited by
Sorted by citations
Zhou, W., Ke, S. Q., Huang, Z., Flavahan, W., Fang, X., Paul, J., Wu, L., Sloan, A. E., McLendon, R. E., Li, X., et al. (2015) · Nature Cell Biology · doi:10.1038/ncb3090 · Cited by 940 · see citing works
Inflammation: Gearing the journey to cancer
Kundu, J. K., & Surh, Y. (2008) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2008.03.002 · Cited by 804 · see citing works
“factors that increase vascular permeability [209–211].”
Inflammation and necrosis promote tumour growth
Vakkila, J., & Lotze, M. T. (2004) · Nature reviews. Immunology · doi:10.1038/nri1415 · Cited by 692 · see citing works
Chemical Biology of the Sugar Code
Gabius, H., Siebert, H., André, S., Jiménez‐Barbero, J., & Rüdiger, H. E. F. (2004) · ChemBioChem · doi:10.1002/cbic.200300753 · Cited by 523 · see citing works
Ryder, M., Ghossein, R. A., Ricarte‐Filho, J. C., Knauf, J. A., & Fagin, J. A. (2008) · Endocrine Related Cancer · doi:10.1677/erc-08-0036 · Cited by 447 · see citing works
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Mast cells: the JEKYLL and HYDE of tumor growth
Theoharides, T. C., & Conti, P. (2004) · Trends in Immunology · doi:10.1016/j.it.2004.02.013 · Cited by 352 · see citing works
Ben‐Baruch, A. (2005) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2005.07.006 · Cited by 336 · see citing works
Anticancer nanomedicine and tumor vascular permeability; Where is the missing link?
Taurin, S., Nehoff, H. L., & Greish, K. F. (2012) · Journal of Controlled Release · doi:10.1016/j.jconrel.2012.07.013 · Cited by 309 · see citing works
27-Hydroxycholesterol Is an Endogenous Selective Estrogen Receptor Modulator
DuSell, C. D., Umetani, M., Shaul, P. W., Mangelsdorf, D. J., & McDonnell, D. P. (2007) · Molecular Endocrinology · doi:10.1210/me.2007-0383 · Cited by 298 · see citing works
LaMontagne, K. R., Littlewood-Evans, A. J., Schnell, C., O’Reilly, T., Wyder, L., Sánchez, T., Probst, B., Butler, J., Wood, A. W., Liau, G., et al. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-2001 · Cited by 295 · see citing works
“matory cells can also promote angiogenesis and tumor growth (32),”
Iron as a central player and promising target in cancer progression
Jung, M., Mertens, C., Tomat, E., & Brüne, B. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20020273 · Cited by 268 · see citing works
“Of note, the appearance of tumor-supporting, iron-donating immune cells, in particular macrophages, is associated with tumor size and aggressiveness as well as poor patient prognosis [56,57].”
BackgroundThe multifaceted roles of chemokines in malignancy
Ben‐Baruch, A. (2006) · Cancer and Metastasis Reviews · doi:10.1007/s10555-006-9003-5 · Cited by 258 · see citing works
“In breast carcinoma, high counts of TAM in the tumors are significantly correlated with clinical aggressiveness, high tumor grade and poor prognosis [28, 34–38].”
BackgroundLymphangiogenesis and lymphatic metastasis in breast cancer
Ran, S., Volk, L. D., Hall, K. L., & Flister, M. J. (2009) · Pathophysiology · doi:10.1016/j.pathophys.2009.11.003 · Cited by 250 · see citing works
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Nanoparticles for modulating tumor microenvironment to improve drug delivery and tumor therapy
Yang, S., & Gao, H. (2017) · Pharmacological Research · doi:10.1016/j.phrs.2017.05.004 · Cited by 256 · see citing works
The immune system and inflammation in breast cancer
Jiang, X., & Shapiro, D. J. (2013) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2013.06.003 · Cited by 243 · see citing works
“Other cells, such as bone marrow-derived Tie2 expressing monocytes (TEMs), tumor associated neutrophils (TANs), immature dendritic cells (DCs) and mast cells all plays roles in breast cancer angiogenesis (Yu and Rak, 2003; De Palma et al., 2005; Fainaru et al., 2010; Gregory and Houghton, 2011).”
BackgroundAngiogenesis in prostate cancer: onset, progression and imaging
Russo, G., Mischi, M., Scheepens, W. A., de la Rosette, J. J. M. C. H., & Wijkstra, H. (2012) · British Journal of Urology · doi:10.1111/j.1464-410x.2012.11444.x · Cited by 196 · see citing works
Farnsworth, R. H., Lackmann, M., Achen, M. G., & Stacker, S. A. (2013) · Oncogene · doi:10.1038/onc.2013.304 · Cited by 192 · see citing works
Veinotte, C. J., Dellaire, G., & Berman, J. N. (2014) · Disease Models & Mechanisms · doi:10.1242/dmm.015784 · Cited by 168 · see citing works
“A number of studies have highlighted the impact of the tumor microenvironment on the proliferation and migration of a variety of human cancers (Gupta and Massagué, 2006; Hanahan et al., 2000; Yu and Rak, 2003).”
BackgroundEterno, V., Zambelli, A., Pavesi, L., Villani, L., Zanini, V., Petrolo, G., Manera, S., Tuscano, A., & Amato, A. M. (2013) · Oncotarget · doi:10.18632/oncotarget.1359 · Cited by 160 · see citing works
“However, it was found that a well orchestrated inflammatory response supports tumorigenesis, creating an optimal microenvironment where cancer cells are continuously stimulated to proliferate, also by recruitment of several cell types able to promote tumor neoangiogenesis [4, 5].”
BackgroundNitric oxide, apoptosis and macrophage polarization during tumor progression
Weigert, A., & Brüne, B. (2008) · Nitric Oxide · doi:10.1016/j.niox.2008.04.021 · Cited by 148 · see citing works
Ran, S., & Montgomery, K. E. (2012) · Cancers · doi:10.3390/cancers4030618 · Cited by 131 · see citing works
“Chronic inflammation is a hallmark of breast cancer [187,188] and has been repeatedly linked to increased tumorigenesis [189,190], angiogenesis [191,192], lymphangiogenesis [65,193] and metastatic progression [194–196].”
BackgroundChemokine Networks and Breast Cancer Metastasis
Karnoub, A. E., & Weinberg, R. A. (2007) · Breast Disease · doi:10.3233/bd-2007-26107 · Cited by 130 · see citing works
“Enhanced leukocyte and stromal infiltrates within tumors almost always signify enhanced tumor vascularity [96].”
Pistelli, M., Lisa, M. D., Ballatore, Z., Caramanti, M., Pagliacci, A., Battelli, N., Ridolfi, F., Santoni, M., Maccaroni, E., Bracci, R., et al. (2015) · BMC Cancer · doi:10.1186/s12885-015-1204-2 · Cited by 119 · see citing works
Taroni, P., Torricelli, A. M., Spinelli, L., Pifferi, A., Arpaia, F., Danesini, G. M., & Cubeddu, R. (2005) · Physics in Medicine and Biology · doi:10.1088/0031-9155/50/11/003 · Cited by 116 · see citing works
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Common Molecular Mechanisms of Mammary Gland Development and Breast Cancer
Lanigan, F. T., O’Connor, D. P., Martin, F., & Gallagher, W. M. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-7386-2 · Cited by 105 · see citing works
Macrophage iron homeostasis and polarization in the context of cancer
Jung, M., Mertens, C., & Brüne, B. (2014) · Immunobiology · doi:10.1016/j.imbio.2014.09.011 · Cited by 103 · see citing works
“Precisely, TAM reflect a panel of different subpopulations of the oversimplified binary M1/M2 scenario and share features of both types with a greater overall similarity to macrophages involved in developmental processes (Ojalvo et al. 2010).”
BackgroundInfluentialExtratumoral Macrophages Promote Tumor and Vascular Growth in an Orthotopic Rat Prostate Tumor Model
Bergström, S. H., Rudolfsson, S. H., van Rooijen, N., & Bergh, A. R. J. (2009) · Neoplasia · doi:10.1593/neo.81338 · Cited by 100 · see citing works
“Several of these factors have been shown to be produced by macrophages (for reviews, see [5,17]), and staining of MMP-9 and IL-1β in the tumors showed that both these proteins were located in macrophage-like cells, particularly at the invasive border.”
BackgroundThe relationship between hypoxia and angiogenesis
Moeller, B. J., Cao, Y., Vujašković, Ž., Li, C. Y., Haroon, Z. A., & Dewhirst, M. W. (2004) · Seminars in Radiation Oncology · doi:10.1016/j.semradonc.2004.04.005 · Cited by 97 · see citing works
Perspectives for Clinical Translation of Adipose Stromal/Stem Cells
Patrikoski, M., Mannerström, B., & Miettinen, S. (2019) · Stem Cells International · doi:10.1155/2019/5858247 · Cited by 93 · see citing works
Murri, A. M. A., Hilmy, M., Bell, J., Wilson, C., McNicol, A. M., Lannigan, A., Doughty, J., & McMillan, D. C. (2008) · British Journal of Cancer · doi:10.1038/sj.bjc.6604667 · Cited by 81 · see citing works
“However, this immune response, in particular the local environment of cytokines, proteases, angiogenic/growth factors and the resulting systemic inflammatory response, may, in turn, stimulate tumour growth and metastasis (O’Sullivan and Lewis, 1994; Leek et al, 1996; Yu and Rak, 2003; Lin and Pollard, 2007).”
BackgroundChandrashekar, N., Asokkumar, S., Subramanian, R., Anandakumar, P., & Devaki, T. (2012) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2012.02.004 · Cited by 79 · see citing works
Minimal Contribution of Marrow-Derived Endothelial Precursors to Tumor Vasculature
Larrivée, B., Niessen, K. S., Pollet, I. L., Corbel, S. Y., Long, M., Rossi, F. M. V., Olive, P. L., & Karsan, A. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.5.2890 · Cited by 77 · see citing works
“It is also possible that VEGF-induced activation of VEGFR-2, even though it does not induce mobilization of endothelial progenitors per se, can promote the expansion and mobilization of myeloid cells such as macrophages, which in turn can actively promote tumor growth through their close interaction with tumor endothe…”
BackgroundZijlmans, H. J. M. A. A., Fleuren, G. J., Baelde, H. J., Eilers, P. H. C., Kenter, G. G., & Gorter, A. (2006) · The Journal of Pathology · doi:10.1002/path.1918 · Cited by 76 · see citing works
Transactivation of MCP‐1/CCL2 by β‐catenin/TCF‐4 in human breast cancer cells
Mestdagt, M., Polette, M., Butticè, G., Noël, A., Ueda, A., Foidart, J., & Gilles, C. (2005) · International Journal of Cancer · doi:10.1002/ijc.21291 · Cited by 76 · see citing works
“It has been particularly implicated in processes characterized by mononuclear cell infiltration including breast cancer.(4,5) In some models, MCP-1 has been shown to display an antitumoral effect.”
BackgroundSystematic review: The oncological safety of adipose fat transfer after breast cancer surgery
Waked, K., Colle, J., Doornaert, M. A. J., Cocquyt, V., & Blondeel, P. N. (2016) · The Breast · doi:10.1016/j.breast.2016.11.001 · Cited by 74 · see citing works
“Experimental studies have pointed out that they can promote tumour growth through several pathways such as enhancing the proliferation and survival of cancer cells, supporting the tumour vasculature, and sustaining a chronic inflammatory state in which tissue regeneration is stimulated [15,25,34,45,64].”
BackgroundThe Tumor Microenvironment: Key to Early Detection
Ariztia, E. V., Lee, C. J., Gogoi, R. P., & Fishman, D. A. (2006) · Critical Reviews in Clinical Laboratory Sciences · doi:10.1080/10408360600778836 · Cited by 71 · see citing works
Jung, M., Weigert, A., Tausendschön, M., Mora, J., Ören, B., Solà, A., Hotter, G., Muta, T., & Brüne, B. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.00413-12 · Cited by 71 · see citing works
“The functional TAM phenotype is at least in part a response to tumor-released components, such as interleukin 10 (IL-10), transforming growth factor (TGF- ), prostanglandin E2 (PGE2), other chemokines, and tumor hypoxia (19).”
BackgroundVascular Growth in Health and Disease
Persson, A. B., & Buschmann, I. R. (2011) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2011.00014 · Cited by 69 · see citing works
Interleukin-6 Increases Expression and Secretion of Cathepsin B by Breast Tumor-Associated Monocytes
Mohamed, M. M., Cavallo‐Medved, D., Rudy, D., Anbalagan, A., Moin, K., & Sloane, B. F. (2010) · Cellular Physiology and Biochemistry · doi:10.1159/000276564 · Cited by 66 · see citing works
Peng, S. (2005) · World Journal of Gastroenterology · doi:10.3748/wjg.v11.i41.6521 · Cited by 66 · see citing works
“. Tumor infi ltrating infl ammatory cells in the microenvironment plays very important functions in tumor angiogenesis [ 6-8 ]”
BackgroundA Critical Role for the Inflammatory Response in a Mouse Model of Preneoplastic Progression
Schwertfeger, K. L., Xian, W., Kaplan, A. M., Burnett, S. H., Cohen, D. A., & Rosen, J. M. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3781 · Cited by 66 · see citing works
“Studies of human breast cancer have shown that increased TAM density predicts poor prognosis and is associated with increased VEGF expression and microvessel density (36, 37), suggesting that macrophages may be involved in tumor angiogenesis.”
BackgroundBarrera, I., & Spiegel, D. (2014) · International Review of Psychiatry · doi:10.3109/09540261.2013.864259 · Cited by 75 · see citing works
“Immune and tumour cell secretion of cytokines (i.e. IL-8) and angiogenic factors (i.e. VEGF) have been associated with increased metastasis (Yu & Rak, 2003).”
BackgroundMammary Gland Macrophages: Pleiotropic Functions in Mammary Development
Schwertfeger, K. L., Rosen, J. M., & Cohen, D. A. (2006) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-006-9028-y · Cited by 61 · see citing works
Annexin 1: Differential expression in tumor and mast cells in human larynx cancer
Silistino‐Souza, R., Rodrigues‐Lisoni, F. C., Cury, P. M., Maniglia, J. V., Raposo, L. S., Tajara, E. H., Christian, H., & Oliani, S. M. (2007) · International Journal of Cancer · doi:10.1002/ijc.22639 · Cited by 59 · see citing works
A Comparative Approach of Tumor-Associated Inflammation in Mammary Cancer between Humans and Dogs
Carvalho, M. I., Silva-Carvalho, R., Pires, I. C. R., Prada, J., Bianchini, R., Jensen‐Jarolim, E., & QUEIROGA, F. L. (2016) · BioMed Research International · doi:10.1155/2016/4917387 · Cited by 57 · see citing works
“Furthermore, some of these proinflammatory mediators directly stimulate the migration and proliferation of endothelial cells, thus promoting angiogenesis and consequently tumor growth [10, 38].”
Psychoneurological symptom cluster in breast cancer: the role of inflammation and diet
George, M. A., Lustberg, M. B., & Orchard, T. (2020) · Breast Cancer Research and Treatment · doi:10.1007/s10549-020-05808-x · Cited by 56 · see citing works
Patel, S. K., Zhang, Y., Pollock, J. A., & Janjic, J. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055802 · Cited by 55 · see citing works
“The tumor environment contains a wide variety of inflammatory cells such as mast cells, dendritic cells, natural killer cells and macrophages [2].”
BackgroundTumor microenvironment and breast cancer progression
Artacho-Cordón, A., Artacho‐Cordón, F., Ríos‐Arrabal, S., Calvente, I., & Núñez, M. I. (2012) · Cancer Biology & Therapy · doi:10.4161/cbt.13.1.18869 · Cited by 50 · see citing works
“Tumor-associated macrophages (TAMs) are a major component of the leukocyte infiltrate, and activated macrophages have been shown to exert both direct and indirect tumoricidal action.(88) Studies on their function using different mouse models of breast cancer revealed that macrophages are required to regulate both the…”
BackgroundImaging and quantifying the dynamics of tumor-associated proteolysis
Sameni, M., Cavallo‐Medved, D., Dosescu, J., Jedeszko, C., Moin, K., Mullins, S., Olive, M. B., Rudy, D., & Sloane, B. F. (2008) · Clinical & Experimental Metastasis · doi:10.1007/s10585-008-9218-7 · Cited by 50 · see citing works
Carvalho, M. I., Pires, I. C. R., Prada, J., Gregório, H., Lobo, L., & QUEIROGA, F. L. (2016) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2016.06.006 · Cited by 49 · see citing works
Conditioning solid tumor microenvironment through inflammatory chemokines and S100 family proteins
Nasser, M. W., Elbaz, M., Ahirwar, D. K., & Ganju, R. K. (2015) · Cancer Letters · doi:10.1016/j.canlet.2015.05.002 · Cited by 48 · see citing works
“ing breast cancer [142,143].”
Endothelins in breast tumour cell invasion
Grimshaw, M. J. (2004) · Cancer Letters · doi:10.1016/j.canlet.2004.08.029 · Cited by 48 · see citing works
Microenvironmental influences on mutagenesis in mammary epithelial cells
Papp-Szabó, E., Josephy, P. D., & Coomber, B. L. (2005) · International Journal of Cancer · doi:10.1002/ijc.21088 · Cited by 47 · see citing works
Pattern response of dendritic cells in the tumor microenvironment and breast cancer
da Cunha, A. (2014) · World Journal of Clinical Oncology · doi:10.5306/wjco.v5.i3.495 · Cited by 45 · see citing works
Anti-angiogenic effect of the total flavonoids in Scutellaria barbata D. Don
Dai, Z.-J., Lu, W.-F., Gao, J., Kang, H., Ma, Y., Zhang, S.-Q., Diao, Y., Lin, S., Wang, X.-J., & Wu, W. (2013) · BMC Complementary and Alternative Medicine · doi:10.1186/1472-6882-13-150 · Cited by 45 · see citing works
“Previous studies have suggested that these inflammatory cells promote the neoplastic progression by stimulating tumor revascularization and other processes related to tumor angiogenesis [31].”
BackgroundYang, M. G., Meng, J., Cheng, X., Lei, J., Guo, H., Zhang, W., Kong, H., & Xu, H. (2012) · Theranostics · doi:10.7150/thno.3629 · Cited by 45 · see citing works
“Extensive research has demonstrated that macrophages in the tumor microenvironment are closely associated with the development and progression of a variety of tumors, such as breast cancer [4-5], prostate [6], glioma [7], lymphoma [8], bladder [9], lung [10], cervical [11] and melanoma [12].”
BackgroundShishido‐Hara, Y., Kurata, A., Fujiwara, M., Itoh, H., Imoto, S., & Kamma, H. (2010) · Diagnostic Pathology · doi:10.1186/1746-1596-5-55 · Cited by 44 · see citing works
“Microenvironments, with secretion of cytokines, seem to affect progression of breast cancer [9,10], and may also determine whether OGCs are formed.”
BackgroundRole of Prolactin and Vasoinhibins in the Regulation of Vascular Function in Mammary Gland
Clapp, C., Thébault, S. C., & de la Escalera, G. M. (2008) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-008-9067-7 · Cited by 43 · see citing works
“Because immune cells contribute to mammary gland involution after lactation [3] and are critical for breast cancer progression [90], the stimulation by PRL to release proangiogenic factors probably influences the way these cells regulate the normal and malignant mammary gland.”
BackgroundBergström, S. H., Hammarsten, P., Adamo, H. H., Wikström, P., & Bergh, A. R. J. (2010) · Expert Opinion on Medical Diagnostics · doi:10.1517/17530059.2011.540009 · Cited by 42 · see citing works
Kim, J. H., Hur, J. H., Lee, S. M., Im, K.-S., Kim, N., & Sur, J. (2011) · The Veterinary Journal · doi:10.1016/j.tvjl.2011.10.022 · Cited by 42 · see citing works
Klement, H., Croix, B. S., Milsom, C., May, L. L., Guo, Q., Yu, J., Klement, P., & Rak, J. W. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2007.070298 · Cited by 41 · see citing works
“It is thought provoking that many cellular components of the angiogenic circuitry in cancer (eg, endothelial or inflammatory cells) are also profoundly affected by the atherosclerotic process and other aspects of vascular aging.(13) This could be of considerable significance for the efficacy of anticancer therapies in…”
Tumor-Associated Macrophages as Targets for Tumor Immunotherapy
Weigert, A., Sekar, D., & Brüne, B. (2008) · Immunotherapy · doi:10.2217/1750743x.1.1.83 · Cited by 40 · see citing works
Kim, J. H., Yu, C.-H., Yhee, J. Y., Im, K.-S., & Sur, J. (2009) · Journal of Comparative Pathology · doi:10.1016/j.jcpa.2009.10.023 · Cited by 38 · see citing works
Dong, L., Yuan, Y., Opansky, C., Chen, Y., Aguilera‐Barrantes, I., Wu, S., Yuan, R., Cao, Q., Cheng, Y. C., Sahoo, D., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.15123 · Cited by 38 · see citing works
“Stimulating microvascular remodeling that may lead to de novo tumor arteriogenesis rather than increasing microvascular density [15, 35, 36] could play a key role in the malignant progression of BCs.”
BackgroundResultInfluentialMartı́nez-Poveda, B., Garcia‐Vilas, J. A., Cárdenas, C., Melgarejo, E., Quesada, A. R., & Medina, M. Á. (2013) · PLoS ONE · doi:10.1371/journal.pone.0055203 · Cited by 38 · see citing works
d’Onofrio, A., Gandolfi, A., & Rocca, A. (2009) · Cell Proliferation · doi:10.1111/j.1365-2184.2009.00595.x · Cited by 38 · see citing works
Continuous Delivery of IFN-β Promotes Sustained Maturation of Intratumoral Vasculature
Dickson, P. V., Hamner, J. B., Streck, C. J., Ng, C. Y., McCarville, M. B., Calabrese, C. R., Gilbertson, R. J., Stewart, C. F., Wilson, C., Gaber, M. W., et al. (2007) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-06-0259 · Cited by 37 · see citing works
“Using this approach, we have identified an additional activity not previously ascribed to IFN-h, that being arterialization of the intratumoral vessels, a process characterized by remodeling and maturation of the vasculature of established tumors (13).”
MethodAngiopoietin/Tie2 signaling, tumor angiogenesis and inflammatory diseases
Kobayashi, H. (2005) · Frontiers in bioscience · doi:10.2741/1561 · Cited by 35 · see citing works
“The infiltrated inflammatory cells promote the formation and enlargement of peritumoral lymphatic vessels, and contribute to tumor to metastasize to distant organs (100).”
BackgroundLiu, J., Wang, P., Zhang, P., Zhang, X., Du, H., Liu, Q., Huang, B., Qian, C., Zhang, S., Zhu, W., et al. (2019) · Journal of Applied Genetics · doi:10.1007/s13353-019-00507-w · Cited by 33 · see citing works
Ren, B., Rose, J. B., Liu, Y., Jaskula‐Sztul, R., Contreras, C. M., Beck, A. W., & Chen, H. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8111980 · Cited by 32 · see citing works
“The significant increase in intratumoral capillaries during tumor progression [89,90] reasonably requires the concurrent expansion of upstream arterioles [20,55,89,91].”
BackgroundTyrosine kinase inhibitors of VEGF receptors: clinical issues and remaining questions
van Cruijsen, H. (2009) · Frontiers in bioscience · doi:10.2741/3377 · Cited by 31 · see citing works
Vicioso, L., Gonzalez, F. J., Alvarez, M., Ribelles, N., Molina, M., Márquez, A., Pérez, L. M. G., Matilla, A., & Alba, E. (2005) · American Journal of Clinical Pathology · doi:10.1309/0864af2u3lgpcf3j · Cited by 31 · see citing works
Diodovich, C., Bianchi, M. G., Bowe, G., Acquati, F., Taramelli, R., Parent‐Massin, D., & Gribaldo, L. (2004) · Toxicology · doi:10.1016/j.tox.2004.03.021 · Cited by 31 · see citing works
Live-cell imaging of tumor proteolysis: Impact of cellular and non-cellular microenvironment
Rothberg, J. M., Sameni, M., Moin, K., & Sloane, B. F. (2011) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2011.07.025 · Cited by 29 · see citing works
“There is an extensive literature [155–168] on the role of the tumor microenvironment in promoting breast tumor progression.”
BackgroundRole of monocyte‐lineage cells in prostate cancer cell invasion and tissue factor expression
Lindholm, P. F., Lü, Y., Adley, B. P., Vladislav, I. T., Jovanovic, B. D., Sivapurapu, N., Yang, X. J., & Kajdacsy‐Balla, A. (2010) · The Prostate · doi:10.1002/pros.21202 · Cited by 28 · see citing works
Owen, J. L., Criscitiello, M. F., Libreros, S., Garcia‐Areas, R., Guthrie, K. M., Torroella‐Kouri, M., & Iragavarapu‐Charyulu, V. (2011) · Cellular Immunology · doi:10.1016/j.cellimm.2011.05.004 · Cited by 28 · see citing works
“Enhanced leukocyte infiltration of tumors has been associated with increased tumor vascularity [64].”
BackgroundAronica, S. M., Raiber, L., Hanzly, M. I., & Kisela, C. (2008) · Journal of Interferon & Cytokine Research · doi:10.1089/jir.2008.0034 · Cited by 27 · see citing works
“Several studies have shown that cancerous tumors can produce increased amounts of VEGF, which, in turn stimulate the proliferation and migration of endothelial cells (Bachelder and others 2002; Yu and Rak 2003).”
A Basis for Distinguishing Cultured Dendritic Cells and Macrophages in Cytospins and Fixed Sections
Vakkila, J., Lotze, M. T., Riga, C., & Jaffe, R. (2005) · Pediatric and Developmental Pathology · doi:10.1007/s10024-004-5045-2 · Cited by 27 · see citing works
“complex, and substantial evidence supports the notion that they actually promote tumour growth [24,30].”
BackgroundTumor Angiogenic Inhibition Triggered Necrosis (TAITN) in Oral Cancer
Yoshida, S., Kawai, H., Eguchi, T., Sukegawa, S., Oo, M. W., Chang, A., Takabatake, K., Nakano, K., Okamoto, K., & Nagatsuka, H. (2019) · Cells · doi:10.3390/cells8070761 · Cited by 26 · see citing works
“Blood vessels generally supply oxygen and nutrients crucial for tumor growth [28,29].”
BackgroundAge‐related properties of the tumour vasculature in renal cell carcinoma
Meehan, B., Appu, S., Croix, B. S., Rak‐Poznanska, K., Klotz, L., & Rak, J. W. (2010) · British Journal of Urology · doi:10.1111/j.1464-410x.2010.09569.x · Cited by 26 · see citing works
Clinical relevance of circulating midkine in ulcerative colitis
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“Also, the recruitment of inflammatory cells secreting angiogenic factors indirectly supports angiogenesis (37).”
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Collateral Growth in the Peripheral Circulation: A Review
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“In addition, consumption of energy-dense foods contributes to the likelihood of increased adiposity which, in turn, is linked to chronic inflammation and increased risk of cancer (5, 28, 29).”
BackgroundSerum levels of angiogenic cytokines decrease after radiotherapy in non-Hodgkin lymphomas
Ria, R., Cirulli, T., Giannini, T., Bambace, S., Serio, G., Portaluri, M. G. A., Ribatti, D., Vacca, A., & Dammacco, F. (2008) · Clinical and Experimental Medicine · doi:10.1007/s10238-008-0170-2 · Cited by 24 · see citing works
“mast cells [4] and macrophages [5], and stimulate resting endothelial cells by means of cognate-specific tyrosinekinase receptors [2].”
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“Angiogenesis is crucial in the growth and spread of malignant mammary tumors [38, 39].”
BackgroundResultInhibition of the HIF-1 Survival Pathway as a Strategy to Augment Photodynamic Therapy Efficacy
de Keijzer, M. J., de Klerk, D. J., de Haan, L. R., van Kooten, R. T., Franchi, L. P., Dias, L. M., Kleijn, T. G., van Doorn, D. J., Heger, M., & on behalf of the Photodynamic Therapy Study Group (2022) · Methods in molecular biology · doi:10.1007/978-1-0716-2099-1_19 · Cited by 12 · see citing works
Spontaneous regression of pancreatic cancer
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Time‐lapse microscopy of macrophages during embryonic vascular development
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Tumor Development Under Combination Treatments with Anti-angiogenic Therapies
Ledzewicz, U., d’Onofrio, A., & Schättler, H. (2012) · Lecture notes on mathematical modelling in the life sciences · doi:10.1007/978-1-4614-4178-6_11 · Cited by 10 · see citing works
“complex process driven by pro-angiogenic factors that are being released as the tumor cells lack a full level of nutrients [66].”
Background
- Authors
- Yu, J. L., & Rak, J. W.
- Affiliations
- McMaster University (CA)
- Corresponding author
- Rak, Janusz W
- Venue
- Breast Cancer Research
- Published
- 2003-04
- Volume
- 5
- Issue
- 2
- Pages
- 83-8
- ISSN
- 1465-5411 (ISSN-L)
- 1465-542X
- PMC
- PMC154151
- OpenAlex
- W1860557886
- Cited by
- 146
- References
- 88
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 1 · 2023: 2 · 2022: 2 · 2021: 1 · 2020: 4 · 2019: 7 · 2018: 1 · 2017: 4 · 2016: 8 · 2015: 7 · 2014: 7 · 2013: 10 · 2012: 13
- FWCI
- 0.83
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Breast Cancer Research (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Cancer Institute
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- breast cancer, tumor microenvironment, tumor angiogenesis, arteriogenesis, inflammatory cells, immune cells, macrophages, MCP-1, endothelial cells, stromal cells, growth factors, proteolytic enzymes
- MeSH terms
- Animals, Blood Vessels, Breast Neoplasms, Humans, Lymphokines, Macrophages, Monocytes, Neovascularization, Pathologic, Macrophage Colony-Stimulating Factor, Endothelial Growth Factors, Chemokine CCL2, Intercellular Signaling Peptides and Proteins, Vascular Endothelial Growth Factors, Vascular Endothelial Growth Factor A
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