Distinct role of macrophages in different tumor microenvironments
Abstract
Macrophages are prominent in the stromal compartment of virtually all types of malignancy. These highly versatile cells respond to the presence of stimuli in different parts of tumors with the release of a distinct repertoire of growth factors, cytokines, chemokines, and enzymes that regulate tumor growth, angiogenesis, invasion, and/or metastasis. The distinct microenvironments where tumor-associated macrophages (TAM) act include areas of invasion where TAMs promote cancer cell motility, stromal and perivascular areas where TAMs promote metastasis, and avascular and perinecrotic areas where hypoxic TAMs stimulate angiogenesis. This review will discuss the evidence for differential regulation of TAMs in these microenvironments and provide an overview of current attempts to target or use TAMs for therapeutic purposes. (Cancer Res 2006; 66(2): 605-12)
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Most tumour-associated macrophages (TAM) adopt an M2-type phenotype, and their presence correlates with poor prognosis.
“Most tumour-associated macrophages (TAM) adopt an M2-type phenotype, and their presence correlates with a poor prognosis [199,200].”
From Superoxide Anion Chemistry—Its Role at the Core of the Innate Immunity (2023) · cites this paper as [199]
In cancer, M1 macrophages have anti-tumour functions, while M2 macrophages support angiogenesis, invasion and metastasis of neoplastic cells.
“In cancer, M1 macrophages have anti-tumour functions, while M2 macrophages support angiogenesis, invasion and metastasis of neoplastic cells.”
From Superoxide Anion Chemistry—Its Role at the Core of the Innate Immunity (2023) · cites this paper as [199]
Cites
MANTOVANI, A., SOZZANI, S., LOCATI, M., ALLAVENA, P., & SICA, A. (2002) · Trends in Immunology · doi:10.1016/s1471-4906(02)02302-5 · Cited by 5,528 · see citing works
Tumour-educated macrophages promote tumour progression and metastasis
Pollard, J. W. (2004) · Nature reviews. Cancer · doi:10.1038/nrc1256 · Cited by 3,365 · see citing works
Self-citationHIF-1α is essential for myeloid cell-mediated inflammation
Cramer, T., Yamanishi, Y., Clausen, B. E., Förster, I., Pawlinski, R., Mackman, N., Haase, V. H., Jaenisch, R., Corr, M., Nizet, V., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)00154-5 · Cited by 2,046 · see citing works
Bingle, L., Brown, N. J., & Lewis, C. E. (2002) · The Journal of Pathology · doi:10.1002/path.1027 · Cited by 2,022 · see citing works
Self-citationColony-Stimulating Factor 1 Promotes Progression of Mammary Tumors to Malignancy
Lin, E. Y., Nguyen, A. V., Russell, R. G., & Pollard, J. W. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.193.6.727 · Cited by 1,594 · see citing works
Self-citationDe Palma, M., Venneri, M. A., Galli, R., Sergi, L. S., Politi, L. S., Sampaolesi, M., & Naldini, L. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.08.002 · Cited by 1,311 · see citing works
Wyckoff, J. B., Wang, W., Lin, E. Y., Wang, Y., Pixley, F. J., Stanley, E. R., Graf, T., Pollard, J. W., Segall, J. E., & Condeelis, J. S. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-1449 · Cited by 1,189 · see citing works
Self-citationAssociation of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma.
Leek, R., Lewis, C. E., Whitehouse, R. M., Greenall, M. J., Clarke, J., & Harris, A. L. (1996) · PubMed · Cited by 1,187 · see citing works
Self-citationKinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation
Winkler, F., Kozin, S. V., Tong, R. T., Chae, S.-S., Booth, M. F., Garkavtsev, I., Xu, L., Hicklin, D. J., Fukumura, D., di Tomaso, E., et al. (2004) · Cancer Cell · doi:10.1016/j.ccr.2004.10.011 · Cited by 1,170 · see citing works
Murdoch, C., Giannoudis, A., & Lewis, C. E. (2004) · Blood · doi:10.1182/blood-2004-03-1109 · Cited by 911 · see citing works
Self-citationHiratsuka, S., Nakamura, K., Iwai, S., Murakami, M., Itoh, T., Kijima, H., Shipley, J. M., Senior, R. M., & Shibuya, M. (2002) · Cancer Cell · doi:10.1016/s1535-6108(02)00153-8 · Cited by 910 · see citing works
Schoppmann, S. F., Birner, P., Stöckl, J., Kalt, R., Ullrich, R., Caucig, C., Kriehuber, E., Nagy, K., Alitalo, K., & Kerjaschki, D. (2002) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)64255-1 · Cited by 794 · see citing works
Goswami, S. K., Sahai, E. A., Wyckoff, J. B., Cammer, M., Cox, D., Pixley, F. J., Stanley, E. R., Segall, J. E., & Condeelis, J. S. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-1853 · Cited by 739 · see citing works
Giraudo, E., Inoue, M., & Hanahan, D. (2004) · Journal of Clinical Investigation · doi:10.1172/jci200422087 · Cited by 700 · see citing works
WINKLER, F., Kozin, S. V., Tong, R. T., Chae, S.-K., Booth, M., Garkavtsev, I., Xu, L., Hicklin, D. J., Fukumura, D., & DiTomaso, E. (2004) · Cancer Cell · doi:10.1016/s1535-6108(04)00305-8 · Cited by 685 · see citing works
Farinha, P., Masoudi, H., Skinnider, B., Shumansky, K., Spinelli, J. J., Gill, K. K., Klasa, R. J., Voss, N., Connors, J. M., & Gascoyne, R. D. (2005) · Blood · doi:10.1182/blood-2005-04-1565 · Cited by 460 · see citing works
Leek, R., Landers, R. J., Harris, A. L., & Lewis, C. E. (1999) · British Journal of Cancer · doi:10.1038/sj.bjc.6690158 · Cited by 450 · see citing works
Self-citationMacrophages Induce Invasiveness of Epithelial Cancer Cells Via NF-κB and JNK
Hagemann, T., Wilson, J. L., Kulbe, H., Li, N. F., Leinster, D. A., Charles, K. A., Klemm, F., Pukrop, T., Binder, C. R., & Balkwill, F. R. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.2.1197 · Cited by 433 · see citing works
Tumor-induced immune dysfunction: the macrophage connection
Elgert, K. D., Alleva, D. G., & Mullins, D. W. (1998) · Journal of Leukocyte Biology · doi:10.1002/jlb.64.3.275 · Cited by 426 · see citing works
Macrophage Responses to Hypoxia
Lewis, C., & Murdoch, C. (2005) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)62038-x · Cited by 413 · see citing works
Self-citationGordon, S. (1986) · Journal of Cell Science · doi:10.1242/jcs.1986.supplement_4.16 · Cited by 411 · see citing works
Hagemann, T. (2004) · Carcinogenesis · doi:10.1093/carcin/bgh146 · Cited by 373 · see citing works
Mitsiades, N., Yu, W., Poulaki, V., Tsokos, M., & Stamenkovic, I. (2001) · PubMed · Cited by 368 · see citing works
Tsutsui, S., Yasuda, K., Suzuki, K., Tahara, K., Higashi, H., & Era, S. (2005) · Oncology Reports · doi:10.3892/or.14.2.425 · Cited by 368 · see citing works
Tumor-Associated Macrophages in Breast Cancer
Leek, R., & Harris, A. L. (2002) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1023/a:1020304003704 · Cited by 353 · see citing works
Huang, S. (2002) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/94.15.1134 · Cited by 345 · see citing works
Negus, R. P. M., Stamp, G. W. H., Hadley, J., & Balkwill, F. R. (1997) · Europe PMC (PubMed Central) · Cited by 341 · 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
Lissbrant, I. F., Stattin, P. E., Wikström, P., Damber, J., Egevad, L., & Bergh, A. R. J. (2000) · International Journal of Oncology · doi:10.3892/ijo.17.3.445 · Cited by 333 · see citing works
Macrophage-derived angiogenesis factors
Sunderkötter, C. H., Goebeler, M., Schulze-Osthoff, K., Bhardwaj, R. S., & Sorg, C. (1991) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(91)90077-y · Cited by 328 · see citing works
Production of Vascular Endothelial Growth Factor by Murine Macrophages
Xiong, M., Elson, G., Legarda, D., & Leibovich, S. J. (1998) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65601-5 · Cited by 306 · see citing works
Nishie, A., Ono, M., Shono, T., Fukushi, J., Otsubo, M., Onoue, H., Ito, Y., Inamura, T., 清信, 池., Fukui, M., et al. (1999) · PubMed · Cited by 301 · see citing works
Immunoregulation by interleukin-12
Trinchieri, G., & Gerosa, F. (1996) · Journal of Leukocyte Biology · doi:10.1002/jlb.59.4.505 · Cited by 295 · see citing works
Hypoxia-Induced Gene Expression in Human Macrophages
Burke, B., Giannoudis, A., Corke, K. P., Gill, D., Wells, M., Ziegler-Heitbrock, L., & Lewis, C. E. (2003) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)63483-9 · Cited by 286 · see citing works
Self-citationCytokine regulation of angiogenesis in breast cancer: the role of tumor-associated macrophages
Lewis, C. E., Leek, R., Harris, A. L., & McGee, J. O. (1995) · Journal of Leukocyte Biology · doi:10.1002/jlb.57.5.747 · Cited by 286 · see citing works
Self-citationPrognostic value of tumor‐associated macrophage count in human bladder cancer
Hanada, T., Nakagawa, M., Emoto, A., Nomura, T., Nasu, N., & Nomura, Y. (2000) · International Journal of Urology · doi:10.1046/j.1442-2042.2000.00190.x · Cited by 284 · see citing works
Aharinejad, S., Paulus, P., Sioud, M., Hofmann, M., Zins, K., Schäfer, R., Stanley, E. R., & Abraham, D. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-0961 · Cited by 280 · see citing works
Macrophage Infiltration and Heme Oxygenase-1 Expression Correlate with Angiogenesis in Human Gliomas
西江, 昭. (2001) · Medical Entomology and Zoology · doi:10.11501/3181003 · Cited by 278 · see citing works
Tumor-infiltrating macrophages (CD68(+) cells) and prognosis in malignant uveal melanoma.
Mäkitie, T., Summanen, P. A., Tarkkanen, A. H. A., & Kivelä, T. (2001) · PubMed · Cited by 273 · see citing works
Tang, Y., Kesavan, P., Nakada, M. T., & Li, Y. (2004) · Molecular Cancer Research · doi:10.1158/1541-7786.73.2.2 · Cited by 257 · see citing works
Reversal of Tumor-Induced Immunosuppression: A New Approach to Cancer Therapy
Wojtowicz‐Praga, S. (1997) · Journal of Immunotherapy · doi:10.1097/00002371-199705000-00001 · Cited by 242 · see citing works
Trochon-Joseph, V., Mabilat, C., Bertrand, P., Legrand, Y., Smadja‐Joffe, F., Soria, C., Delpech, B., & Lu, H. (1996) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19960529)66:5 · Cited by 211 · see citing works
Mediation of Wound-Related Rous Sarcoma Virus Tumorigenesis by TGF-β
Sieweke, M. H., Thompson, N. L., Sporn, M. B., & Bissell, M. J. (1990) · Science · doi:10.1126/science.2163544 · Cited by 207 · see citing works
The macrophage – a novel system to deliver gene therapy to pathological hypoxia
Griffiths, L. G., Binley, K. E., Iqball, S., Kan, O., Maxwell, P. H., Ratcliffe, P. J., Lewis, C. E., Harris, A. L., Kingsman, S. M., & Naylor, S. (2000) · Gene Therapy · doi:10.1038/sj.gt.3301058 · Cited by 206 · see citing works
Self-citationPrognostic significance of CD8+ T cell and macrophage peritumoral infiltration in colorectal cancer
Funada, Y., Noguchi, T., 菊池, 隆., et al. (2003) · Oncology Reports · doi:10.3892/or.10.2.309 · Cited by 205 · see citing works
Klimp, A. H., Hollema, H., Kempinga, C., van der Zee, A. G. J., de Vries, E. G. E., & Daemen, T. (2001) · PubMed · Cited by 199 · see citing works
Macrophages promote angiogenesis in human breast tumour spheroids in vivo
Bingle, L., Lewis, C. E., Corke, K. P., Reed, M., & Brown, N. J. (2005) · British Journal of Cancer · doi:10.1038/sj.bjc.6602901 · Cited by 190 · see citing works
Self-citationOhno, S., Ohno, Y., Suzuki, N., Kamei, T., Koike, K., Inagawa, H., Kohchi, C., Soma, G., & Inoue, M. (2004) · PubMed · Cited by 184 · see citing works
Matrilysin (MMP-7) promotes invasion of ovarian cancer cells by activation of progelatinase
Wang, F.-Q., So, J., Reierstad, S., & Fishman, D. A. (2004) · International Journal of Cancer · doi:10.1002/ijc.20697 · Cited by 182 · see citing works
Ohno, S., Inagawa, H., Dhar, D. K., et al. (2004) · PubMed · Cited by 173 · see citing works
Burke, B., Tang, N., Corke, K. P., Tazzyman, D., Ameri, K., Wells, M. W., & Lewis, C. E. (2001) · The Journal of Pathology · doi:10.1002/path.1029 · Cited by 169 · see citing works
Self-citationPiras, F., Colombari, R., Minerba, L., Murtas, D., Floris, C., Maxia, C., Corbu, A., Perra, M. T., & Sirigu, P. (2005) · Cancer · doi:10.1002/cncr.21283 · Cited by 169 · see citing works
Matrilysin [MMP-7] Expression Selects for Cells with Reduced Sensitivity to Apoptosis
Fingleton, B., Vargo-Gogola, T. C., Crawford, H. C., & Matrisian, L. M. (2001) · Neoplasia · doi:10.1038/sj.neo.7900190 · Cited by 158 · see citing works
Koide, N., Nishio, A., Sato, T., Sugiyama, A., & Miyagawa, S.-I. (2004) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2004.30733.x · Cited by 158 · see citing works
Secretion of epidermal growth factor by macrophages associated with breast carcinoma
O'Sullivan, C., Lewis, C. E., McGee, J., & Harris, A. L. (1993) · The Lancet · doi:10.1016/0140-6736(93)91348-p · Cited by 157 · see citing works
Self-citationKhorana, A. A., Ryan, C., Cox, C., Eberly, S. W., & Sahasrabudhe, D. M. (2003) · Cancer · doi:10.1002/cncr.11152 · Cited by 152 · see citing works
White, J. R., Harris, R. A., Lee, S. R., Craigon, M., Binley, K. M., Price, T., Beard, G. L., Mundy, C. R., & Naylor, S. (2003) · Genomics · doi:10.1016/s0888-7543(03)00215-5 · Cited by 139 · see citing works
Immune cell infiltrates and prognosis in primary carcinoma of the lung
Johnson, S. K., Kerr, K. M., Chapman, A. D., et al. (2000) · Lung Cancer · doi:10.1016/s0169-5002(99)00095-1 · Cited by 134 · see citing works
Macrophages direct tumour histology and clinical outcome in a colon cancer model
Oosterling, S. J., van der Bij, G. J., Meijer, G. A., et al. (2005) · The Journal of Pathology · doi:10.1002/path.1830 · Cited by 125 · see citing works
Clinical effects of tumor-associated macrophages and dendritic cells on renal cell carcinoma.
Hamada, I., Kato, M., Yamasaki, T., Iwabuchi, K., Watanabe, T., Yamada, T., Itoyama, S., Ito, H., & Okada, K. (2002) · PubMed · Cited by 101 · see citing works
The mononuclear cell infiltrate compared with survival in high-grade astrocytomas
Rossi, M. I., Jones, N., Candy, E., Nicoll, J. A. R., Compton, J. S., Hughes, J. T., Esiri, M. M., Moss, T., Cruz-Sánchez, F. F., & Coakham, H. B. (1989) · Acta Neuropathologica · doi:10.1007/bf00688208 · Cited by 78 · see citing works
Jadus, M., Irwin, M., Irwin, M., et al. (1996) · Blood · doi:10.1182/blood.v87.12.5232.bloodjournal87125232 · Cited by 74 · see citing works
Augmentation of metastasis formation by thioglycollate‐elicited macrophages
Gorelik, E., Wiltrout, R. H., Brunda, M. J., et al. (1982) · International Journal of Cancer · doi:10.1002/ijc.2910290514 · Cited by 73 · see citing works
Satoh, T., Saika, T., Ebara, S., et al. (2003) · PubMed · Cited by 70 · see citing works
Öberg, Å., Samii, S., Stenling, R., et al. (2001) · International Journal of Colorectal Disease · doi:10.1007/s003840100337 · Cited by 66 · see citing works
Mitsuhashi, M., Liu, J., Cao, S., Shi, X., & Ma, X. (2004) · Journal of Leukocyte Biology · doi:10.1189/jlb.1203641 · Cited by 62 · see citing works
Domagała, W., Striker, G., Szadowska, A., et al. (1992) · PubMed · Cited by 61 · see citing works
Effects of extracellular pH on tumour necrosis factor-α production by resident alveolar macrophages
Heming, T. A., DAVÉ, S. K., TUAZON, D. M., Chopra, A. K., Peterson, J. W., & Bidani, A. (2001) · Clinical Science · doi:10.1042/cs1010267 · Cited by 60 · see citing works
Nishizuka, I., Ichikawa, Y., Ishikawa, T., Kamiyama, M., Hasegawa, S., Momiyama, N., Miyazaki, K., & Shimada, H. (2001) · Cancer Letters · doi:10.1016/s0304-3835(01)00634-6 · Cited by 57 · see citing works
Davidson, B., Goldberg, I., Gotlieb, W. H., Lerner‐Geva, L., Ben‐Baruch, G., Agulansky, L., Novikov, I., & Kopolovic, J. (1999) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1034/j.1600-0412.1999.780312.x · Cited by 43 · see citing works
Gene expression profiling using laser capture microdissection
Todd, R., & Kuo, M. W. L. W. P. (2002) · Expert Review of Molecular Diagnostics · doi:10.1586/14737159.2.5.497 · Cited by 39 · see citing works
Jadus, M. R., Williams, C. C., Avina, M. D., et al. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.160.1.361 · Cited by 37 · see citing works
Macrophage-tumour cell associations in breast cancer
van Netten, J., George, E., Ashmead, B. J., et al. (1993) · The Lancet · doi:10.1016/0140-6736(93)92734-b · Cited by 29 · see citing works
Effect of macrophage depletion on growth and neovascularization of hamster buccal pouch carcinomas
Polverini, P. J., & Leibovich, S. J. (1987) · Journal of Oral Pathology and Medicine · doi:10.1111/j.1600-0714.1987.tb00714.x · Cited by 23 · see citing works
Davidson, B., Goldberg, I., Gotlieb, W. H., et al. (1999) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1080/j.1600-0412.1999.780312.x · Cited by 19 · see citing works
Cathepsin D in invasive ductal NOS breast carcinoma as defined by immunohistochemistry
Domagała, W., Striker, G., Szadowska, A., et al. (1992) · Cited by 14 · see citing works
Zeineddine, N. S., Avina, M. D., Williams, C. C., et al. (1999) · Immunology Letters · doi:10.1016/s0165-2478(99)00129-7 · Cited by 11 · see citing works
Ross, J. A., & Auger, M. J. (2002) · doi:10.1093/oso/9780192631978.003.0001 · Cited by 10 · see citing works
Hewlett, G., Opitz, H.-G., Flad, H. D., et al. (1979) · The Journal of Immunology · doi:10.4049/jimmunol.123.5.2265 · Cited by 6 · see citing works
Jadus, M. R., Williams, C. C., Ly, M., et al. (1997) · Journal of Immunotherapy · doi:10.1097/00002371-199709000-00089 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Immunity, Inflammation, and Cancer
Grivennikov, S. I., Greten, F. R., & Karin, M. (2010) · Cell · doi:10.1016/j.cell.2010.01.025 · Cited by 10,755 · see citing works
Accessories to the Crime: Functions of Cells Recruited to the Tumor Microenvironment
Hanahan, D., & Coussens, L. M. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.02.022 · Cited by 4,632 · see citing works
Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm
Biswas, S. K., & Mantovani, A. (2010) · Nature Immunology · doi:10.1038/ni.1937 · Cited by 3,840 · see citing works
Microenvironmental regulation of metastasis
Joyce, J. A., & Pollard, J. W. (2009) · Nature Reviews Cancer · doi:10.1038/nrc2618 · Cited by 3,684 · see citing works
Self-citationHypoxia-inducible factors and the response to hypoxic stress
Majmundar, A. J., Wong, W. J., & Simon, M. C. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.09.022 · Cited by 2,380 · see citing works
Lin, Y., Xu, J., & Lan, H. (2019) · Journal of Hematology & Oncology · doi:10.1186/s13045-019-0760-3 · Cited by 1,398 · see citing works
IL-6 in inflammation, autoimmunity and cancer
Hirano, T. (2021) · International Immunology · doi:10.1093/intimm/dxaa078 · Cited by 1,453 · see citing works
Broz, M. L., Binnewies, M., Boldajipour, B., Nelson, A. E., Pollack, J. L., Erle, D. J., Barczak, A., Rosenblum, M. D., Daud, A., Barber, D. L., et al. (2014) · Cancer Cell · doi:10.1016/j.ccell.2014.09.007 · Cited by 1,207 · see citing works
Genin, M., Clement, F., Fattaccioli, A., Raes, M., & Michiels, C. (2015) · BMC Cancer · doi:10.1186/s12885-015-1546-9 · Cited by 1,090 · see citing works
Macrophage Regulation of Tumor Responses to Anticancer Therapies
De Palma, M., & Lewis, C. E. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.02.013 · Cited by 1,079 · see citing works
Self-citationMacrophages in Tumor Microenvironments and the Progression of Tumors
Hao, N.-B., Lü, M.-H., Fan, Y.-H., Cao, Y.-L., Zhang, Z.-R., & Yang, S.-M. (2012) · Clinical and Developmental Immunology · doi:10.1155/2012/948098 · Cited by 1,003 · see citing works
Extracellular matrix and its therapeutic potential for cancer treatment
Huang, J., Zhang, L., Wan, D., Zhou, L., Zheng, S., Lin, S., & Qiao, Y. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00544-0 · Cited by 962 · see citing works
Sinha, P., Clements, V. K., Bunt, S. K., Albelda, S. M., & Ostrand-Rosenberg, S. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.2.977 · Cited by 847 · see citing works
The Role of Cancer-Associated Fibroblasts and Fibrosis in Liver Cancer
Affo, S., Yu, L.-X., & Schwabe, R. F. (2017) · Annual Review of Pathology: Mechanisms of Disease · doi:10.1146/annurev-pathol-052016-100322 · Cited by 757 · see citing works
Qian, B., Deng, Y., Im, J. H., Muschel, R. J., Zou, Y., Li, J., Lang, R. A., & Pollard, J. W. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006562 · Cited by 664 · see citing works
Self-citationStromal cells in tumor microenvironment and breast cancer
Mao, Y., Keller, E. T., Garfield, D. H., Shen, K., & Wang, J. (2013) · Cancer and Metastasis Reviews · doi:10.1007/s10555-012-9415-3 · Cited by 671 · see citing works
Multifunctional polymeric micelles for delivery of drugs and siRNA
Jhaveri, A. M., & Torchilin, V. P. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00077 · Cited by 466 · see citing works
Imtiyaz, H. Z., Williams, E. P., Hickey, M. M., Patel, S. A., Durham, A. C., Yuan, L.-J., Hammond, R., Gimotty, P. A., Keith, B., & Simon, M. C. (2010) · Journal of Clinical Investigation · doi:10.1172/jci39506 · Cited by 461 · see citing works
Macrophage-derived exosome-mimetic hybrid vesicles for tumor targeted drug delivery
Rayamajhi, S., Nguyen, T. D. T., Marasini, R., & Aryal, S. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.05.054 · Cited by 429 · see citing works
Kidd, S., Spaeth, E., Watson, K., Burks, J., Lu, H., Klopp, A., Andreeff, M., & Marini, F. C. (2012) · PLoS ONE · doi:10.1371/journal.pone.0030563 · Cited by 371 · see citing works
Mechanisms regulating T-cell infiltration and activity in solid tumors
Lanitis, E., Dangaj, D., Irving, M., & Coukos, G. (2017) · Annals of Oncology · doi:10.1093/annonc/mdx238 · Cited by 369 · see citing works
Harnessing tumor‐associated macrophages as aids for cancer immunotherapy
Li, X., Liu, R., Su, X., Pan, Y., Han, X., Shao, C., & Shi, Y. (2019) · Molecular Cancer · doi:10.1186/s12943-019-1102-3 · Cited by 364 · see citing works
Tissue homeostasis and inflammation
Meizlish, M. L., Franklin, R. A., Zhou, X., & Medzhitov, R. (2021) · Annual Review of Immunology · doi:10.1146/annurev-immunol-061020-053734 · Cited by 364 · see citing works
Macrophages: An Inflammatory Link Between Angiogenesis and Lymphangiogenesis
Corliss, B. A., Azimi, M. S., Munson, J. M., Peirce, S. M., & Murfee, W. L. (2016) · Microcirculation · doi:10.1111/micc.12259 · Cited by 356 · see citing works
Cancer immunoediting by the innate immune system in the absence of adaptive immunity
O’Sullivan, T., Saddawi-Konefka, R., Vermi, W., Koebel, C. M., Arthur, C., White, J. M., Uppaluri, R., Andrews, D. M., Ngiow, S. F., Teng, M. W. L., et al. (2012) · Journal of Experimental Medicine · doi:10.1084/jem.20112738 · Cited by 348 · see citing works
Superoxide Anion Chemistry—Its Role at the Core of the Innate Immunity
Andrés, C. M. C., Pérez de la Lastra, J. M., Andrés Juan, C., Plou, F. J., & Pérez-Lebeña, E. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24031841 · Cited by 342 · see citing works
From mice to humans: developments in cancer immunoediting
Teng, M. W. L., Galon, J., Fridman, W.-H., & Smyth, M. J. (2015) · Journal of Clinical Investigation · doi:10.1172/jci80004 · Cited by 337 · see citing works
Fang, H.-Y., Hughes, R., Murdoch, C., Coffelt, S. B., Biswas, S. K., Harris, A. L., Johnson, R. S., Imityaz, H. Z., Simon, M. C., Fredlund, E., et al. (2009) · Blood · doi:10.1182/blood-2008-12-195941 · Cited by 319 · see citing works
Self-citationExpression of Tie-2 by Human Monocytes and Their Responses to Angiopoietin-2
Murdoch, C., Tazzyman, S., Webster, S., & Lewis, C. E. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.11.7405 · Cited by 318 · see citing works
Self-citationYang, J., Liao, D., Chen, C., Liu, Y., Chuang, T.-H., Xiang, R., Markowitz, D., Reisfeld, R. A., & Luo, Y. (2013) · Stem Cells · doi:10.1002/stem.1281 · Cited by 301 · see citing works
A mouse-human phase 1 co-clinical trial of a protease-activated fluorescent probe for imaging cancer
Whitley, M. J., Cardona, D. M., Lazarides, A. L., Spasojevic, I., Ferrer, J. M., Cahill, J., Lee, C.-L., Snuderl, M., Blazer, D. G., Hwang, E. S., et al. (2016) · Science Translational Medicine · doi:10.1126/scitranslmed.aad0293 · Cited by 296 · see citing works
“The labeling of tumor-associated macrophages likely occurs because these cells also express high levels of proteases (24), and the intraoperative identification and removal of these cells may, in fact, be beneficial to patients because these cells are associated with tumor progression and metastasis (25, 26).”
BackgroundHorwitz, S. M., Koch, R., Porcu, P., Oki, Y., Moskowitz, A., Perez, M., Myskowski, P., Officer, A., Jaffe, J. D., Morrow, S. N., et al. (2018) · Blood · doi:10.1182/blood-2017-08-802470 · Cited by 290 · see citing works
Fujimoto, H., Sangai, T., Ishii, G., Ikehara, A., Nagashima, T., Miyazaki, M., & Ochiai, A. (2009) · International Journal of Cancer · doi:10.1002/ijc.24378 · Cited by 263 · see citing works
Edris, B., Weiskopf, K., Volkmer, A. K., Volkmer, J.-P., Willingham, S. B., Contreras-Trujillo, H., Liu, J., Majeti, R., West, R. B., Fletcher, J. A., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1121629109 · Cited by 258 · see citing works
Angiopoietin‐2: a multifaceted cytokine that functions in both angiogenesis and inflammation
Scholz, A., Plate, K. H., & Reiss, Y. (2015) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12726 · Cited by 248 · see citing works
Heymann, M.-F., Lézot, F., & Heymann, D. (2019) · Cellular Immunology · doi:10.1016/j.cellimm.2017.10.011 · Cited by 233 · see citing works
Non-genetic engineering of cells for drug delivery and cell-based therapy
Wang, Q., Cheng, H., Peng, H., Zhou, H., Li, P. Y., & Langer, R. (2015) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2014.12.003 · Cited by 225 · see citing works
Antonios, J. P., Soto, H., Everson, R. G., Moughon, D., Orpilla, J. R., Shin, N. P., Sedighim, S., Treger, J., Odesa, S., Tucker, A., et al. (2017) · Neuro-Oncology · doi:10.1093/neuonc/now287 · Cited by 206 · see citing works
Secreted protein lipocalin‐2 promotes microglial M1 polarization
Jang, E., Lee, S., Kim, J., Kim, J., Seo, J., Lee, W., Mori, K., Nakao, K., & Suk, K. (2013) · The FASEB Journal · doi:10.1096/fj.12-222257 · Cited by 198 · see citing works
Kharaishvili, G., Simkova, D., Bouchalova, K., Gachechiladze, M., Narsia, N., & Bouchal, J. (2014) · Cancer Cell International · doi:10.1186/1475-2867-14-41 · Cited by 197 · see citing works
Osteoclasts are important for bone angiogenesis
Cackowski, F. C., Anderson, J. L., Patrene, K. D., Choksi, R. J., Shapiro, S. D., Windle, J. J., Blair, H. C., & Roodman, G. D. (2010) · Blood · doi:10.1182/blood-2009-08-237628 · Cited by 188 · see citing works
Functional plasticity of macrophages: in situ reprogramming of tumor-associated macrophages
Stout, R. D., Watkins, S. K., & Suttles, J. (2009) · Journal of Leukocyte Biology · doi:10.1189/jlb.0209073 · Cited by 183 · see citing works
Huang, B.-W., & Gao, J.-Q. (2018) · Journal of Controlled Release · doi:10.1016/j.jconrel.2017.12.005 · Cited by 174 · see citing works
TGF-β-induced IRAK-M expression in tumor-associated macrophages regulates lung tumor growth
Standiford, T. J., Kuick, R., Bhan, U., Chen, J., Newstead, M., & Keshamouni, V. G. (2011) · Oncogene · doi:10.1038/onc.2010.619 · Cited by 151 · see citing works
Iron in the Tumor Microenvironment-Connecting the Dots
Pfeifhofer-Obermair, C., Tymoszuk, P., Petzer, V., Weiss, G., & Nairz, M. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00549 · Cited by 151 · see citing works
Angiogenesis, adipokines and breast cancer
Vona-Davis, L., & Rose, D. P. (2009) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2009.05.007 · Cited by 148 · see citing works
Cyp4a in tumor-associated macrophages promotes pre-metastatic niche formation and metastasis
Chen, X. W., Yu, T. J., Zhang, J., Li, Y., Chen, H. L., Yang, G. F., Yu, W., Liu, Y. Z., Liu, X. X., Duan, C. F., et al. (2017) · Oncogene · doi:10.1038/onc.2017.118 · Cited by 143 · see citing works
Tumor-Derived Adenosine Promotes Macrophage Proliferation in Human Hepatocellular Carcinoma
Wang, J., Wang, Y., Chu, Y., Li, Z., Yu, X., Huang, Z., Xu, J., & Zheng, L. (2021) · Journal of Hepatology · doi:10.1016/j.jhep.2020.10.021 · Cited by 133 · see citing works
STAT3, a master regulator of anti-tumor immune response
Rébé, C., & Ghiringhelli, F. (2019) · Cancers · doi:10.3390/cancers11091280 · Cited by 129 · see citing works
Zhang, Y., Sun, Y., Rao, E., Yan, F., Li, Q., Zhang, Y., Silverstein, K. A. T., Liu, S., Sauter, E., Cleary, M. P., et al. (2014) · Cancer Research · doi:10.1158/0008-5472.can-13-2689 · Cited by 129 · see citing works
Metastasis in context: modeling the tumor microenvironment with cancer-on-a-chip approaches
Sleeboom, J. J. F., Eslami Amirabadi, H., Nair, P., Sahlgren, C. M., & den Toonder, J. M. J. (2018) · Disease Models & Mechanisms · doi:10.1242/dmm.033100 · Cited by 122 · see citing works
The M2a macrophage subset may be critically involved in the fibrogenesis of endometriosis in mice
Duan, J., Liu, X., Wang, H., & Guo, S.-W. (2018) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2018.05.017 · Cited by 121 · see citing works
Li, B., Vincent, A., Cates, J., Brantley-Sieders, D. M., Polk, D. B., & Young, P. P. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-1565 · Cited by 115 · see citing works
Circulating CD14+CD16+ monocyte levels predict tissue invasive character of cholangiocarcinoma
Subimerb, C., Pinlaor, S., Lulitanond, V, Khuntikeo, N., Okada, S., McGrath, M. S., & Wongkham, S. (2010) · Clinical and Experimental Immunology · doi:10.1111/j.1365-2249.2010.04200.x · Cited by 113 · see citing works
Characterizing the role of monocytes in T cell cancer immunotherapy using a 3d microfluidic model
Lee, S. W. L., Adriani, G., Ceccarello, E., Pavesi, A., Tan, A. T., Bertoletti, A., Kamm, R. D., & Wong, S. C. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00416 · Cited by 109 · see citing works
Li, R., Hebert, J. D., Lee, T. A., Xing, H., Boussommier-Calleja, A., Hynes, R. O., Lauffenburger, D. A., & Kamm, R. D. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-0442 · Cited by 100 · see citing works
Regulation of efferocytosis as a novel cancer therapy
Zhou, Y., Yao, Y., Deng, Y., & Shao, A. (2020) · Cell Communication and Signaling · doi:10.1186/s12964-020-00542-9 · Cited by 100 · see citing works
Angiogenesis induced by controlled release of neuropeptide substance P
Kohara, H., Tajima, S., Yamamoto, M., & Tabata, Y. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.07.079 · Cited by 99 · see citing works
Wagner, M., Bjerkvig, R., Wiig, H., Melero-Martin, J. M., Lin, R.-Z., Klagsbrun, M., & Dudley, A. C. (2012) · Angiogenesis · doi:10.1007/s10456-012-9276-y · Cited by 91 · see citing works
CD47 blockade inhibits tumor progression human osteosarcoma in xenograft models
Xu, J.-F., Pan, X.-H., Zhang, S.-J., Zhao, C., Qiu, B.-S., Gu, H.-F., Hong, J.-F., Cao, L., Chen, Y., Xia, B., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.4282 · Cited by 88 · see citing works
Mertens, C., Akam, E. A., Rehwald, C., Brüne, B., Tomat, E., & Jung, M. (2016) · PLOS ONE · doi:10.1371/journal.pone.0166164 · Cited by 83 · see citing works
Mulrooney, T. J., Marsh, J., Urits, I., Seyfried, T. N., & Mukherjee, P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018085 · Cited by 75 · see citing works
Lee, S. W. L., Seager, R. J., Litvak, F., Spill, F., Sieow, J. L., Leong, P. H., Kumar, D., Tan, A. S. M., Wong, S. C., Adriani, G., et al. (2020) · Integrative Biology · doi:10.1093/intbio/zyaa007 · Cited by 60 · see citing works
Elsum, I. A., Yates, L. L., Pearson, H. B., Phesse, T. J., Long, F., O'Donoghue, R., Ernst, M., Cullinane, C., & Humbert, P. O. (2014) · Oncogene · doi:10.1038/onc.2013.498 · Cited by 60 · see citing works
Hypoxia-inducible factors as key regulators of tumor inflammation
Mamlouk, S., & Wielockx, B. (2013) · International Journal of Cancer · doi:10.1002/ijc.27901 · Cited by 61 · see citing works
A 25-gene classifier predicts overall survival in resectable pancreatic cancer
Birnbaum, D. J., Finetti, P., Lopresti, A., Gilabert, M., Poizat, F., Raoul, J.-L., Delpero, J.-R., Moutardier, V., Birnbaum, D., Mamessier, E., et al. (2017) · BMC Medicine · doi:10.1186/s12916-017-0936-z · Cited by 51 · see citing works
Liu, X., Xu, D., Huang, C., Guo, Y., Wang, S., Zhu, C., Xu, J., Zhang, Z., Shen, Y., Zhao, W., et al. (2019) · Journal of Translational Medicine · doi:10.1186/s12967-019-1929-9 · Cited by 53 · see citing works
The Endometriotic Tumor Microenvironment in Ovarian Cancer
Wendel, J. R. H., Wang, X., & Hawkins, S. M. (2018) · Cancers · doi:10.3390/cancers10080261 · Cited by 51 · see citing works
Metabolism in tumour-associated macrophages: a<i>quid pro quo</i>with the tumour microenvironment
Zheng, X., Mansouri, S., Krager, A., Grimminger, F., Seeger, W., Pullamsetti, S. S., Wheelock, C. E., & Savai, R. (2020) · European Respiratory Review · doi:10.1183/16000617.0134-2020 · Cited by 41 · see citing works
Iron imaging reveals tumor and metastasis macrophage hemosiderin deposits in breast cancer
Leftin, A., Ben-Chetrit, N., Klemm, F., Joyce, J. A., & Koutcher, J. A. (2017) · PLOS ONE · doi:10.1371/journal.pone.0184765 · Cited by 36 · see citing works
Nilkhet, S., Mongkolpobsin, K., Sillapachaiyaporn, C., Wongsirojkul, N., Tencomnao, T., & Chuchawankul, S. (2024) · Scientific Reports · doi:10.1038/s41598-024-58208-2 · Cited by 21 · see citing works
Tumor-associated macrophages, angiogenesis, and tumor cell migration in oral squamous cell carcinoma
Ghanaati, S., Udeabor, S., Adisa, A., Orlowska, A., & Sader, R. (2017) · Annals of African Medicine · doi:10.4103/aam.aam_8_17 · Cited by 19 · see citing works
- Authors
- Lewis, C. E., & Pollard, J. W.
- Affiliations
- University of Sheffield (GB)
- Albert Einstein College of Medicine (US)
- Venue
- Cancer Research
- Published
- 2006-01-15
- Volume
- 66
- Issue
- 2
- Pages
- 605-612
- ISSN
- 0008-5472 (ISSN-L)
- 1538-7445
- OpenAlex
- W2131464730
- Cited by
- 2,225
- References
- 81
- Citations by year
- 2026: 24 · 2025: 59 · 2024: 88 · 2023: 112 · 2022: 102 · 2021: 121 · 2020: 147 · 2019: 105 · 2018: 112 · 2017: 117 · 2016: 122 · 2015: 115 · 2014: 152 · 2013: 143 · 2012: 123
- FWCI
- 7.67
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cancer Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Cancer Institute (CA 94173, P01CA100324, R01CA094173, CA 100324, P30CA013330)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- tumor-associated macrophages, tumor microenvironment, tumor stroma, tumor invasion, metastasis, angiogenesis, hypoxia, cytokines and chemokines, TAM-targeted therapy
- MeSH terms
- Cell Movement, Humans, Immunotherapy, Macrophages, Neoplasm Metastasis, Neoplasms, Neovascularization, Pathologic, Disease Progression
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review