Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis
Open accessAbstract
We demonstrate a novel tumor-promoting role of myeloid immune suppressor Gr+CD11b+ cells, which are evident in cancer patients and tumor-bearing animals. These cells constitute approximately 5% of total cells in tumors. Tumors coinjected with Gr+CD11b+ cells exhibited increased vascular density, vascular maturation, and decreased necrosis. These immune cells produce high levels of MMP9. Deletion of MMP9 in these cells completely abolishes their tumor-promoting ability. Gr+CD11b+ cells were also found to directly incorporate into tumor endothelium. Consistent with this observation, Gr+CD11b+ cells acquire endothelial cell (EC) properties in tumor microenvironment and proangiogenic culture conditions. Our data provide evidence that Gr+CD11b+ cells of immune origin induced by tumors directly contribute to tumor growth and vascularization by producing MMP9 and differentiating into ECs.
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BMDCs promote metastasis by producing chemokines that recruit tumor cells to the lung by mechanisms that include stimulation of tumor cell extravasation.
“The BMDCs promote metastasis by producing chemokines that recruit tumor cells to the lung by mechanisms that include stimulation of tumor cell extravasation”
From Hypoxic control of metastasis (2016) · cites this paper as [93]
Cites
Coussens, L. M., & Werb, Z. (2002) · Nature · doi:10.1038/nature01322 · Cited by 15,111 · see citing works
Isolation of Putative Progenitor Endothelial Cells for Angiogenesis
Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T., Witzenbichler, B., Schatteman, G., & Isner, J. M. (1997) · Science · doi:10.1126/science.275.5302.964 · Cited by 8,725 · see citing works
Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis
Bergers, G., Brekken, R., McMahon, G., Vu, T. H., Itoh, T., Tamaki, K., Tanzawa, K., Thorpe, P., Itohara, S., Werb, Z., et al. (2000) · Nature Cell Biology · doi:10.1038/35036374 · Cited by 2,797 · see citing works
Lyden, D., Hattori, K., Dias, S., Costa, C., Blaikie, P., Butros, L., Chadburn, A., Heissig, B., Marks, W., Witte, L., et al. (2001) · Nature Medicine · doi:10.1038/nm1101-1194 · Cited by 1,860 · see citing works
Heissig, B., Hattori, K., Dias, S., Friedrich, M., Ferris, B., Hackett, N. R., Crystal, R. G., Besmer, P., Lyden, D. C., Moore, M. A. S., et al. (2002) · Cell · doi:10.1016/s0092-8674(02)00754-7 · Cited by 1,744 · see citing works
Vu, T. H., Shipley, J. M., Bergers, G., Berger, J. E., Helms, J. A., Hanahan, D., Shapiro, S. D., Senior, R. M., & Werb, Z. (1998) · Cell · doi:10.1016/s0092-8674(00)81169-1 · Cited by 1,737 · see citing works
Carmeliet, P., Moons, L., Luttun, A., Vincenti, V., Compernolle, V., Mol, M. D., Wu, Y., Bono, F., Devy, L., Beck, H., et al. (2001) · Nature Medicine · doi:10.1038/87904 · Cited by 1,673 · see citing works
Little Evidence for Developmental Plasticity of Adult Hematopoietic Stem Cells
Wagers, A. J., Sherwood, R. I., Christensen, J. L., & Weissman, I. L. (2002) · Science · doi:10.1126/science.1074807 · Cited by 1,460 · see citing works
Almand, B., Clark, J. I., Nikitina, E., van Beynen, J., English, N. R., Knight, S. C., Carbone, D. P., & Gabrilovich, D. I. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.1.678 · Cited by 1,340 · see citing works
Self-citationMMP-9 Supplied by Bone Marrow–Derived Cells Contributes to Skin Carcinogenesis
Coussens, L. M., Tinkle, C. L., Hanahan, D., & Werb, Z. (2000) · Cell · doi:10.1016/s0092-8674(00)00139-2 · Cited by 1,306 · see citing works
Origin of endothelial progenitors in human postnatal bone marrow
Reyes, M., Dudek, A. Z., Jahagirdar, B., Koodie, L., Marker, P. H., & Verfaillie, C. M. (2002) · Journal of Clinical Investigation · doi:10.1172/jci14327 · Cited by 1,105 · see citing works
Luttun, A., Tjwa, M., Moons, L., Wu, Y. L., Angelillo‐Scherrer, A., Liao, F., Nagy, J. A., Hooper, A. T., Priller, J., Klerck, B. D., et al. (2002) · Nature Medicine · doi:10.1038/nm731 · Cited by 1,067 · see citing works
Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts
Lyden, D. C., Young, A. Z., Zagzag, D., Yan, W. X., Gerald, W. L., O'Reilly, R., Bader, B., Hynes, R. O., Zhuang, Y., Manova, K., et al. (1999) · Nature · doi:10.1038/44334 · Cited by 912 · see citing works
Hiratsuka, 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
Origin of endothelial progenitors in human postnatal bone marrow
Reyes, M., Dudek, A. Z., Jahagirdar, B., Koodie, L., Marker, P. H., & Verfaillie, C. M. (2002) · Journal of Clinical Investigation · doi:10.1172/jci0214327 · Cited by 887 · see citing works
Hattori, K., Dias, S., Heissig, B., Hackett, N. R., Lyden, D. C., Tateno, M., Hicklin, D. J., Zhu, Z., Witte, L., Crystal, R. G., et al. (2001) · The Journal of Experimental Medicine · doi:10.1084/jem.193.9.1005 · Cited by 685 · see citing works
Vascular and haematopoietic stem cells: novel targets for anti-angiogenesis therapy?
Rafii, S., Lyden, D. C., Benezra, R., Hattori, K., & Heissig, B. (2002) · Nature reviews. Cancer · doi:10.1038/nrc925 · Cited by 678 · see citing works
Hattori, K., Heissig, B., Wu, Y. L., Dias, S., Tejada, R., Ferris, B., Hicklin, D. J., Zhu, Z., Böhlen, P., Witte, L., et al. (2002) · Nature Medicine · doi:10.1038/nm740 · Cited by 632 · see citing works
Hamano, Y., Zeisberg, M., Sugimoto, H., Lively, J. C., Maeshima, Y., Yang, C., Hynes, R. O., Werb, Z., Sudhakar, A., & Kalluri, R. (2003) · Cancer Cell · doi:10.1016/s1535-6108(03)00133-8 · Cited by 560 · see citing works
Palma, M. D., Venneri, M. A., Roca, C., & Naldini, L. (2003) · Nature Medicine · doi:10.1038/nm871 · Cited by 549 · see citing works
Bronte, V., Apolloni, E., Cabrelle, A., Ronca, R., Serafini, P., Zamboni, P., Restifo, N. P., & Zanovello, P. (2000) · Blood · doi:10.1182/blood.v96.12.3838 · Cited by 527 · see citing works
Rodrı́guez-Manzaneque, J. C., Lane, T. F., Ortega, M.-A., Hynes, R. O., Lawler, J., & Iruela‐Arispe, M. L. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.171460498 · Cited by 473 · see citing works
Kusmartsev, S. A., Cheng, F., Yu, B., Nefedova, Y., Sotomayor, E. M., Lush, R. M., & Gabrilovich, D. I. (2003) · PubMed · Cited by 460 · see citing works
Gabrilovich, D. I., Ishida, T., Nadaf, S., Ohm, J. E., & Carbone, D. P. (1999) · PubMed · Cited by 459 · see citing works
Self-citationSchmeißer, A. (2001) · Cardiovascular Research · doi:10.1016/s0008-6363(00)00270-4 · Cited by 423 · 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
Derangement of immune responses by myeloid suppressor cells
Serafini, P., Santo, C. D., Marigo, I., Cingarlini, S., Dolcetti, L., Gallina, G., Zanovello, P., & Bronte, V. (2003) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-003-0443-2 · Cited by 335 · see citing works
Brekken, R. A., Overholser, J. P., Stastny, V., Waltenberger, J. L., Minna, J. D., & Thorpe, P. E. (2000) · PubMed · Cited by 310 · see citing works
Immature myeloid cells and cancer-associated immune suppression
Kusmartsev, S. A., & Gabrilovich, D. I. (2002) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-002-0280-8 · Cited by 297 · see citing works
Melani, C. C., Chiodoni, C., Forni, G., & Colombo, M. P. (2003) · Blood · doi:10.1182/blood-2003-01-0190 · Cited by 295 · see citing works
CD34−Blood‐Derived Human Endothelial Cell Progenitors
Harraz, M. M., Jiao, C., Hanlon, H. D., et al. (2001) · Stem Cells · doi:10.1634/stemcells.19-4-304 · Cited by 289 · see citing works
Chantrain, C. F., Shimada, H., Jodele, S., Groshen, S. G., Ye, W., Shalinsky, D. R., Werb, Z., Coussens, L. M., & DeClerck, Y. A. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-0160 · Cited by 217 · see citing works
Dendritic Cells in Antitumor Immune Responses
Gabrilovich, D. I., Nadaf, S., Corak, J., Berzofsky, J. A., & Carbone, D. P. (1996) · Cellular Immunology · doi:10.1006/cimm.1996.0140 · Cited by 213 · see citing works
Self-citationLin, P. C., Sankar, S., Shan, S. Q., Dewhirst, M. W., Polverini, P. J., Quinn, T. Q., & Peters, K. G. (1998) · PubMed · Cited by 199 · see citing works
Self-citationWitty, J. P., Wright, J. H., & Matrisian, L. M. (1995) · Molecular Biology of the Cell · doi:10.1091/mbc.6.10.1287 · Cited by 192 · see citing works
Self-citationCell surface association of matrix metalloproteinase-9 (gelatinase B)
Fridman, R. A., Tóth, M., Chvyrkova, I., Meroueh, S. O., & Mobashery, S. (2003) · Cancer and Metastasis Reviews · doi:10.1023/a:1023091214123 · Cited by 155 · see citing works
Pujol, B. F., Lucibello, F. C., Zuzarte, M., Lütjens, P., Müller, R., & HAVEMANN, K. (2001) · European Journal of Cell Biology · doi:10.1078/0171-9335-00136 · Cited by 137 · see citing works
Increased primary tumor growth in mice null for β3- or β3/β5-integrins or selectins
Taverna, D., Moher, H., Crowley, D. G., Borsig, L., Varki, A. P., & Hynes, R. O. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0307289101 · Cited by 100 · see citing works
Myeloid progenitor cells mediate immune suppression in patients with head and neck cancers
Young, M. R., & Lathers, D. M. R. (1999) · International Journal of Immunopharmacology · doi:10.1016/s0192-0561(99)00008-9 · Cited by 96 · see citing works
Joshi, C., & Enver, T. (2002) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(02)00392-7 · Cited by 46 · see citing works
Ljung, B., Mayall, B. H., Lottich, C., Boyer, C. M., Sylvester, S. S., Leight, G. S., Siegler, H. F., & Smith, H. S. (1989) · Breast Cancer Research and Treatment · doi:10.1007/bf01806527 · Cited by 32 · see citing works
Kamaté, C., Baloul, S., Grootenboer‐Mignot, S., Pessis, É., Chevrot, A., Tulliez, M., Marchiol, C., Viguier, M., & FRADELIZI, D. (2002) · International Journal of Cancer · doi:10.1002/ijc.10519 · Cited by 29 · see citing works
Flagged first, then by citations
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Myeloid-derived-suppressor cells as regulators of the immune system
Gabrilovich, D. I., & Nagaraj, S. (2009) · Nature Reviews Immunology · doi:10.1038/nri2506 · Cited by 6,753 · see citing works
Primary, Adaptive, and Acquired Resistance to Cancer Immunotherapy
Sharma, P., Hu-Lieskovan, S., Wargo, J. A., & Ribas, A. (2017) · Cell · doi:10.1016/j.cell.2017.01.017 · Cited by 5,588 · see citing works
Orimo, A., Gupta, P. B., Sgroi, D. C., Arenzana-Seisdedos, F., Delaunay, T., Naeem, R., Carey, V. J., Richardson, A. L., & Weinberg, R. A. (2005) · Cell · doi:10.1016/j.cell.2005.02.034 · Cited by 3,759 · see citing works
Modes of resistance to anti-angiogenic therapy
Bergers, G., & Hanahan, D. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2442 · Cited by 2,953 · see citing works
Influence of tumour micro-environment heterogeneity on therapeutic response
Junttila, M. R., & de Sauvage, F. J. (2013) · Nature · doi:10.1038/nature12626 · Cited by 2,694 · see citing works
Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards
Bronte, V., Brandau, S., Chen, S.-H., Colombo, M. P., Frey, A. B., Greten, T. F., Mandruzzato, S., Murray, P. J., Ochoa, A., Ostrand-Rosenberg, S., et al. (2016) · Nature Communications · doi:10.1038/ncomms12150 · Cited by 2,751 · see citing works
Neutrophils in cancer: Neutral no more
Coffelt, S. B., Wellenstein, M. D., & de Visser, K. E. (2016) · Nature reviews. Cancer · doi:10.1038/nrc.2016.52 · Cited by 1,830 · see citing works
Regulation of immune responses by L-arginine metabolism
Bronte, V., & Zanovello, P. (2005) · Nature Reviews Immunology · doi:10.1038/nri1668 · Cited by 1,775 · see citing works
The role of myeloid cells in the promotion of tumour angiogenesis
Murdoch, C., Muthana, M., Coffelt, S. B., & Lewis, C. E. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2444 · Cited by 1,642 · see citing works
Huang, B., Pan, P.-Y., Li, Q., Sato, A. I., Levy, D. E., Bromberg, J., Divino, C. M., & Chen, S.-H. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-1299 · Cited by 1,435 · see citing works
Tumour hypoxia promotes tolerance and angiogenesis via CCL28 and Treg cells
Facciabene, A., Peng, X., Hagemann, I. S., Balint, K., Barchetti, A., Wang, L.-P., Gimotty, P. A., Gilks, C. B., Lal, P., Zhang, L., et al. (2011) · Nature · doi:10.1038/nature10169 · Cited by 1,376 · see citing works
Rankin, E. B., & Giaccia, A. J. (2016) · Science · doi:10.1126/science.aaf4405 · Cited by 1,340 · see citing works
De 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
Cellular Senescence: Aging, Cancer, and Injury
Calcinotto, A., Kohli, J., Zagato, E., Pellegrini, L., Demaria, M., & Alimonti, A. (2019) · Physiological Reviews · doi:10.1152/physrev.00020.2018 · Cited by 1,270 · see citing works
Molecular characterization of the tumor microenvironment in breast cancer
Allinen, M., Beroukhim, R., Cai, L., Brennan, C., Lahti-Domenici, J., Huang, H., Porter, D., Hu, M., Chin, L., Richardson, A., et al. (2004) · Cancer Cell · doi:10.1016/j.ccr.2004.06.010 · Cited by 1,299 · see citing works
Erler, J. T., Bennewith, K. L., Cox, T. R., Lang, G., Bird, D., Koong, A., Le, Q.-T., & Giaccia, A. J. (2009) · Cancer Cell · doi:10.1016/j.ccr.2008.11.012 · Cited by 1,231 · see citing works
History of myeloid-derived suppressor cells
Talmadge, J. E., & Gabrilovich, D. I. (2013) · Nature Reviews Cancer · doi:10.1038/nrc3581 · Cited by 1,148 · see citing works
Immunological hallmarks of stromal cells in the tumour microenvironment
Turley, S. J., Cremasco, V., & Astarita, J. L. (2015) · Nature Reviews Immunology · doi:10.1038/nri3902 · Cited by 1,140 · see citing works
Suzuki, E., Kapoor, V., Jassar, A. S., Kaiser, L. R., & Albelda, S. M. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-0883 · Cited by 1,054 · see citing works
TGF-β and immune cells: an important regulatory axis in the tumor microenvironment and progression
Yang, L., Pang, Y., & Moses, H. L. (2010) · Trends in Immunology · doi:10.1016/j.it.2010.04.002 · Cited by 1,023 · see citing works
Self-citationDynamics of the immune reaction to pancreatic cancer from inception to invasion
Clark, C. E., Hingorani, S. R., Mick, R., Combs, C., Tuveson, D. A., & Vonderheide, R. H. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-0175 · Cited by 990 · see citing works
Bayne, L. J., Beatty, G. L., Jhala, N., Clark, C. E., Rhim, A. D., Stanger, B. Z., & Vonderheide, R. H. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.04.025 · Cited by 947 · see citing works
“Other potential roles of Gr-1 + CD11b + cells in regulating tumor growth (Yang et al., 2004, 2008, 2011) appear therefore to be secondary or noncontributory to tumor growth, at least in this assay.”
BackgroundYang, L., Huang, J., Ren, X., Gorska, A. E., Chytil, A., Aakre, M., Carbone, D. P., Matrisian, L. M., Richmond, A., Lin, P. C., et al. (2008) · Cancer Cell · doi:10.1016/j.ccr.2007.12.004 · Cited by 918 · see citing works
Self-citationTumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells
Shojaei, F., Wu, X., Malik, A. K., Zhong, C., Baldwin, M. E., Schanz, S., Fuh, G., Gerber, H.-P., & Ferrara, N. (2007) · Nature Biotechnology · doi:10.1038/nbt1323 · Cited by 849 · see citing works
Kowanetz, M., Wu, X., Lee, J., Tan, M., Hagenbeek, T., Qu, X., Yu, L., Ross, J., Korsisaari, N., Cao, T., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1015855107 · Cited by 663 · see citing works
Tumor microenvironment: The role of the tumor stroma in cancer
Li, H., Fan, X., & Houghton, J. (2007) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21159 · Cited by 646 · see citing works
KRAS-IRF2 axis drives immune suppression and immune therapy resistance in colorectal cancer
Liao, W., Overman, M. J., Boutin, A. T., Shang, X., Zhao, D., Dey, P., Li, J., Wang, G., Lan, Z., Li, J., et al. (2019) · Cancer Cell · doi:10.1016/j.ccell.2019.02.008 · Cited by 617 · see citing works
Ostrand-Rosenberg, S., Sinha, P., Beury, D. W., & Clements, V. K. (2012) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2012.01.011 · Cited by 583 · see citing works
Butler, J. M., Kobayashi, H., & Rafii, S. (2010) · Nature Reviews Cancer · doi:10.1038/nrc2791 · Cited by 578 · see citing works
Ozao-Choy, J., Ma, G., Kao, J., Wang, G. X., Meseck, M., Sung, M., Schwartz, M., Divino, C. M., Pan, P.-Y., & Chen, S.-H. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-4709 · Cited by 538 · see citing works
Ostrand-Rosenberg, S., & Fenselau, C. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1701019 · Cited by 509 · see citing works
The parallel lives of angiogenesis and immunosuppression: cancer and other tales
Motz, G. T., & Coukos, G. (2011) · Nature Reviews Immunology · doi:10.1038/nri3064 · Cited by 481 · see citing works
Chiu, D. K.-C., Tse, A. P.-W., Xu, I. M.-J., Di Cui, J., Lai, R. K.-H., Li, L. L., Koh, H.-Y., Tsang, F. H.-C., Wei, L. L., Wong, C.-M., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00530-7 · Cited by 448 · see citing works
The pre-metastatic niche: finding common ground
Sceneay, J., Smyth, M. J., & Möller, A. (2013) · Cancer and Metastasis Reviews · doi:10.1007/s10555-013-9420-1 · Cited by 422 · see citing works
Dudley, A. C. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a006536 · Cited by 424 · see citing works
Schmid, M. C., Avraamides, C. J., Dippold, H. C., Franco, I., Foubert, P., Ellies, L. G., Acevedo, L. M., Manglicmot, J. R. E., Song, X., Wrasidlo, W., et al. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.04.016 · Cited by 378 · see citing works
CCL2/CCR2 pathway mediates recruitment of myeloid suppressor cells to cancers
Huang, B., Lei, Z., Zhao, J., Gong, W., Liu, J., Chen, Z., Liu, Y., Li, D., Yuan, Y., Zhang, G.-M., et al. (2007) · Cancer Letters · doi:10.1016/j.canlet.2006.12.012 · Cited by 349 · see citing works
Holmgaard, R. B., Schaer, D. A., Li, Y., Castaneda, S. P., Murphy, M. Y., Xu, X., Inigo, I., Dobkin, J., Manro, J. R., Iversen, P. W., et al. (2018) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-018-0356-4 · Cited by 356 · see citing works
Chiu, D. K., Xu, I. M., Lai, R. K., Tse, A. P., Wei, L. L., Koh, H., Li, L. L., Lee, D., Lo, R. C., Wong, C., et al. (2016) · Hepatology · doi:10.1002/hep.28655 · Cited by 241 · see citing works
Neutrophils: important contributors to tumor progression and metastasis
Swierczak, A., Mouchemore, K. A., Hamilton, J. A., & Anderson, R. L. (2015) · Cancer and Metastasis Reviews · doi:10.1007/s10555-015-9594-9 · Cited by 220 · 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
Noel, M., O’Reilly, E. M., Wolpin, B. M., Ryan, D. P., Bullock, A. J., Britten, C. D., Linehan, D. C., Belt, B. A., Gamelin, E. C., Ganguly, B., et al. (2020) · Investigational New Drugs · doi:10.1007/s10637-019-00830-3 · Cited by 199 · see citing works
van Deventer, H. W., Burgents, J. E., Wu, Q. P., Woodford, R.-M. T., Brickey, W. J., Allen, I. C., McElvania-Tekippe, E., Serody, J. S., & Ting, J. P.-Y. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-1921 · Cited by 172 · see citing works
Transforming Growth Factor β: Tumor Suppressor or Promoter? Are Host Immune Cells the Answer?
Yang, L., & Moses, H. L. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-2556 · Cited by 151 · see citing works
Self-citationChemotherapy and tumor microenvironment of pancreatic cancer
Liu, Q., Liao, Q., & Zhao, Y. (2017) · Cancer Cell International · doi:10.1186/s12935-017-0437-3 · Cited by 120 · 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
Myeloid cell dysfunction and the pathogenesis of the diabetic chronic wound
Wicks, K., Torbica, T., & Mace, K. A. (2014) · Seminars in Immunology · doi:10.1016/j.smim.2014.04.006 · Cited by 93 · see citing works
Yin, T., Zhao, Z.-B., Guo, J., Wang, T., Yang, J.-B., Wang, C., Long, J., Ma, S., Huang, Q., Zhang, K., et al. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-3397 · Cited by 92 · see citing works
Anti-angiogenic effect of high doses of ascorbic acid
Mikirova, N. A., Ichim, T. E., & Riordan, N. H. (2008) · Journal of Translational Medicine · doi:10.1186/1479-5876-6-50 · Cited by 78 · see citing works
Deletion of TGF-β signaling in myeloid cells enhances their anti-tumorigenic properties
Novitskiy, S. V., Pickup, M. W., Chytil, A., Polosukhina, D., Owens, P., & Moses, H. L. (2012) · Journal of Leukocyte Biology · doi:10.1189/jlb.1211639 · Cited by 79 · see citing works
TGFβ and cancer metastasis: an inflammation link
Yang, L. (2010) · Cancer and Metastasis Reviews · doi:10.1007/s10555-010-9226-3 · Cited by 65 · see citing works
Self-citationEpigenetic mechanisms of tumor resistance to immunotherapy
Arenas-Ramirez, N., Sahin, D., & Boyman, O. (2018) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-018-2908-7 · Cited by 36 · see citing works
- Authors
- Yang, L., DeBusk, L. M., Fukuda, K., Fingleton, B., Green-Jarvis, B., Shyr, Y., Matrisian, L. M., Carbone, D. P., & Lin, P. C.
- Affiliations
- Vanderbilt University (US)
- Corresponding author
- Lin, P.Charles
- Venue
- Cancer Cell
- Publisher
- Elsevier BV
- Published
- 2004-10
- Volume
- 6
- Issue
- 4
- Pages
- 409-421
- ISSN
- 1535-6108 (ISSN-L)
- OpenAlex
- W2021268612
- Cited by
- 1,140
- References
- 42
- Citations by year
- 2026: 8 · 2025: 28 · 2024: 34 · 2023: 40 · 2022: 48 · 2021: 60 · 2020: 61 · 2019: 44 · 2018: 57 · 2017: 62 · 2016: 62 · 2015: 62 · 2014: 72 · 2013: 86 · 2012: 73
- FWCI
- 11.32
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cancer Cell (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ca087756-03)
- National Cancer Institute (CA095103, 5P50CA90949, P50CA095103, CA-89674, R01CA076321, CA076321, CA87756, P50CA090949, T32CA009592, R01CA089674)
- 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
- myeloid-derived suppressor cells, tumor angiogenesis, MMP-9, tumor endothelium, endothelial differentiation, tumor microenvironment, vessel density, vascular maturation, tumor necrosis, tumor growth, tumor vascularization
- MeSH terms
- Animals, Bone Marrow, Cell Differentiation, Cells, Cultured, Endothelium, Female, Humans, Necrosis, Neoplasm Transplantation, Neoplasms, Neovascularization, Pathologic, Apoptosis, Mice, Knockout, Disease Progression, Stem Cell Factor, Matrix Metalloproteinase 9, CD11b Antigen, Vascular Endothelial Growth Factor A, Mice
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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.
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