Efferocytosis Creates a Tumor Microenvironment Supportive of Tumor Survival and Metastasis
Open accessAbstract
Programmed cell death, or apoptosis, occurs in nearly all tissues of all multi-cellular organisms. In order to avoid leakage of intracellular contents, which could generate tissue damaging inflammation, apoptotic cells are cleared from tissues by phagocytes, which then dispatch the engulfed dying cell through the lysosomal pathway. Phagocytic clearance of apoptotic cells is referred to as efferocytosis. One key feature of efferocytosis is the production and release of wound healing cytokines by the phagocyte, which acts to resolve inflammation, and promote tissue repair. Phagocytic engulfment of apoptotic cells coupled with cytokine modulation aimed at immune suppression ensures that physiological programmed cell death does not induce inflammation and tissue damage. However, cytokines involved in wound healing and immune suppression are notorious for their role in the tumor microenvironment, increasing tumor cell motility and promoting evasion of anti-tumor immunity. Therefore, current and future studies aimed at targeting important players of efferocytosis should reveal new and efficacious therapeutic approaches for limiting cancer progression and relapse.
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Efferocytosis is seen as a major hurdle to using antigen presenting cells in cell-based therapies.
“It is seen as a major hurdle to using antigen presenting cells in cell-based therapies (61–64).”
From Cholesterol efflux protein, ABCA1, supports anticancer functions of myeloid immune cells (2026) · cites this paper as [62]
The Introduction (page not provided) says efferocytosis causes antigen-presenting macrophages to promote immune tolerance and suppress adaptive immune responses. It does not describe efferocytosis as a major hurdle to using antigen-presenting cells in cell-based therapies; that application and degree of difficulty are unsupported. (LLM, conf=0.78)
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1 retracted
FOXO3 programs tumor-associated DCs to become tolerogenic in human and murine prostate cancer
Watkins, S. K., Zhu, Z., Riboldi, E., Shafer-Weaver, K., Stagliano, K. E., Sklavos, M. M., Ambs, S., Yagita∥, H., & Hurwitz, A. A. (2011) · Journal of Clinical Investigation · doi:10.1172/jci44325 · Cited by 132 · see citing works
RetractedHallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590 · see citing works
PD-1 and PD-L1 Immune Checkpoint Blockade to Treat Breast Cancer
Hartkopf, A. D., Taran, F., Wallwiener, M., Walter, C. B., Krämer, B., Grischke, E., & Brucker, S. Y. (2016) · Breast Care · doi:10.1159/000453569 · Cited by 30,989 · see citing works
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
Exploring the full spectrum of macrophage activation
Mosser, D. M., & Edwards, J. P. (2008) · Nature Reviews Immunology · doi:10.1038/nri2448 · Cited by 9,144 · see citing works
Microenvironmental regulation of tumor progression and metastasis
Quail, D. F., & Joyce, J. A. (2013) · Nature Medicine · doi:10.1038/nm.3394 · Cited by 7,994 · see citing works
Curiel, T. J., Coukos, G., Zou, L., Alvarez, X., Cheng, P., Mottram, P., Evdemon-Hogan, M., Conejo-Garcia, J. R., Zhang, L., Burow, M., et al. (2004) · Nature Medicine · doi:10.1038/nm1093 · Cited by 5,151 · see citing works
Chen, W., Jin, W., Hardegen, N. J., Lei, K.-J., Li, L., Marinos, N. J., McGrady, G., & Wahl, S. M. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20030152 · Cited by 4,678 · see citing works
Tumors: Wounds That Do Not Heal
Flier, J. S., Underhill, L. H., & Dvorak, H. F. (1986) · New England Journal of Medicine · doi:10.1056/nejm198612253152606 · Cited by 4,391 · 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
Coordinated regulation of myeloid cells by tumours
Gabrilovich, D. I., Ostrand-Rosenberg, S., & Bronte, V. (2012) · Nature Reviews Immunology · doi:10.1038/nri3175 · Cited by 3,544 · see citing works
Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J., Bratton, D. L., & Henson, P. M. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.148.7.2207 · Cited by 3,321 · see citing works
Macrophage activation and polarization
Martinez, F. O. (2008) · Frontiers in Bioscience · doi:10.2741/2692 · Cited by 3,160 · see citing works
Martin, S. J., Reutelingsperger, C. P., McGahon, A. J., Rader, J. A., van Schie, R. C., LaFace, D. M., & Green, D. R. (1995) · The Journal of experimental medicine · doi:10.1084/jem.182.5.1545 · Cited by 2,824 · see citing works
Rho GTPases and signaling networksPreprint
Aelst, L. V., & D’Souza‐Schorey, C. (1997) · Genes & Development · doi:10.1101/gad.11.18.2295 · Cited by 2,358 · see citing works
Immunosuppressive Strategies that are Mediated by Tumor Cells
Rabinovich, G. A., Gabrilovich, D. I., & Sotomayor, E. M. (2006) · Annual Review of Immunology · doi:10.1146/annurev.immunol.25.022106.141609 · Cited by 1,699 · see citing works
Identification of a factor that links apoptotic cells to phagocytes
Hanayama, R., Tanaka, M., Miwa, K., Shinohara, A., Iwamatsu, A., & Nagata, S. (2002) · Nature · doi:10.1038/417182a · Cited by 1,401 · 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
Phagocytosis and clearance of apoptotic cells is mediated by MER
Scott, R. S., McMahon, E. J., Pop, S. M., Reap, E. A., Caricchio, R., Cohen, P. L., Earp, H. S., & Matsushima, G. K. (2001) · Nature · doi:10.1038/35075603 · Cited by 1,215 · see citing works
Bates, G. J., Fox, S., Han, C., Leek, R., García, J. F., Harris, A., & Banham, A. (2006) · Journal of Clinical Oncology · doi:10.1200/jco.2006.05.9584 · Cited by 1,209 · see citing works
Identification of Tim4 as a phosphatidylserine receptor
Miyanishi, M., Tada, K., Koike, M., Uchiyama, Y., Kitamura, T., & Nagata, S. (2007) · Nature · doi:10.1038/nature06307 · Cited by 1,180 · 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
Gao, Q., Qiu, S.-J., Fan, J., Zhou, J., Wang, X.-Y., Xiao, Y.-S., Xu, Y., Li, Y.-W., & Tang, Z.-Y. (2007) · Journal of Clinical Oncology · doi:10.1200/jco.2006.09.4565 · Cited by 1,140 · see citing works
TAM Receptors Are Pleiotropic Inhibitors of the Innate Immune Response
Rothlin, C. V., Ghosh, S., Zuniga, E. I., Oldstone, M. B. A., & Lemke, G. (2007) · Cell · doi:10.1016/j.cell.2007.10.034 · Cited by 1,055 · see citing works
Autoimmune Disease and Impaired Uptake of Apoptotic Cells in MFG-E8-Deficient Mice
Hanayama, R., Tanaka, M., Miyasaka, K., Aozasa, K., Koike, M., Uchiyama, Y., & Nagata, S. (2004) · Science · doi:10.1126/science.1094359 · Cited by 992 · see citing works
Salama, P. R., Phillips, M. R., Grieu, F., Morris, M. J., Zeps, N., Joseph, D. J., Platell, C. F. E., & Iacopetta, B. J. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.18.7229 · Cited by 992 · see citing works
The polarization of immune cells in the tumour environment by TGFβ
Flavell, R. A., Sanjabi, S., Wrzesinski, S. H., & Licona-Limón, P. (2010) · Nature Reviews Immunology · doi:10.1038/nri2808 · Cited by 940 · see citing works
Yang, 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
Immunobiology of the TAM receptors
Lemke, G., & Rothlin, C. V. (2008) · Nature reviews. Immunology · doi:10.1038/nri2303 · Cited by 867 · see citing works
BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module
Park, D., Tosello‐Trampont, A., Elliott, M. R., Lu, M., Haney, L. B., Ma, Z., Klibanov, A. L., Mandell, J. W., & Ravichandran, K. S. (2007) · Nature · doi:10.1038/nature06329 · Cited by 848 · see citing works
Lindau, D., Gielen, P. R., Kroesen, M., Wesseling, P., & Adema, G. J. (2012) · Immunology · doi:10.1111/imm.12036 · Cited by 817 · see citing works
Ichimura, T., van Asseldonk, E. J. P., Humphreys, B. D., Gunaratnam, L., Duffield, J. S., & Bonventre, J. V. (2008) · Journal of Clinical Investigation · doi:10.1172/jci34487 · Cited by 768 · see citing works
Linger, R. M. A., Keating, A. K., Earp, H. S., & Graham, D. K. (2008) · Advances in cancer research · doi:10.1016/s0065-230x(08)00002-x · Cited by 750 · see citing works
Myeloid Suppressor Lines Inhibit T Cell Responses by an NO-Dependent Mechanism
Mazzoni, A., Bronte, V., Visintin, A., Spitzer, J. H., Apolloni, E., Serafini, P., Zanovello, P., & Segal, D. M. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.2.689 · Cited by 692 · see citing works
TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells.
Kobayashi, N., Karisola, P., Peña-Cruz, V., Dorfman, D., Jinushi, M., Umetsu, S., Butte, M., Nagumo, H., Chernova, I., Zhu, B., et al. (2007) · Immunity · doi:10.1016/j.immuni.2007.11.011 · Cited by 688 · see citing works
Gal, A., Li, Y., Thompson, D. A., Weir, J., Orth, U., Jacobson, S. G., Apfelstedt-Sylla, E., & Vollrath, D. (2000) · Nature Genetics · doi:10.1038/81555 · Cited by 679 · see citing works
Zizzo, G., Hilliard, B. A., Monestier, M., & Cohen, P. L. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1200662 · Cited by 650 · see citing works
Gumienny, T. L., Brugnera, E., Tosello-Trampont, A.-C., Kinchen, J. M., Haney, L. B., Nishiwaki, K., Walk, S. F., Nemergut, M. E., Macara, I. G., Francis, R., et al. (2001) · Cell · doi:10.1016/s0092-8674(01)00520-7 · Cited by 568 · see citing works
Mechanism of Immune Dysfunction in Cancer Mediated by Immature Gr-1+ Myeloid Cells
Gabrilovich, D. I., Velders, M. P., Sotomayor, E. M., & Kast, W. M. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.9.5398 · Cited by 538 · see citing works
A microRNA regulon that mediates endothelial recruitment and metastasis by cancer cells
Png, K. J., Halberg, N., Yoshida, M., & Tavazoie, S. F. (2011) · Nature · doi:10.1038/nature10661 · Cited by 531 · see citing works
Nosho, K., Baba, Y., Tanaka, N., Shima, K., Hayashi, M., Meyerhardt, J. A., Giovannucci, E., Dranoff, G., Fuchs, C. S., & Ogino, S. (2010) · The Journal of Pathology · doi:10.1002/path.2774 · Cited by 502 · see citing works
CX3CL1/fractalkine is released from apoptotic lymphocytes to stimulate macrophage chemotaxis
Truman, L. A., Ford, C. A., Pasikowska, M., Pound, J. D., Wilkinson, S. J., Dumitriu, I. E., Melville, L., Melrose, L. A., Ogden, C. A., Nibbs, R., et al. (2008) · Blood · doi:10.1182/blood-2008-06-162404 · Cited by 473 · see citing works
Petersen, R., Campa, M. J., Sperlazza, J., Conlon, D. H., Joshi, M., Harpole, D., & Patz, E. (2006) · Cancer · doi:10.1002/cncr.22282 · Cited by 471 · see citing works
Pregnancy-associated breast cancer and metastasis
Schedin, P. S. (2006) · Nature reviews. Cancer · doi:10.1038/nrc1839 · Cited by 467 · see citing works
Rapid cell corpse clearance by stabilin-2, a membrane phosphatidylserine receptor
Park, S.-Y., Jung, M.-Y., Kim, H.-J., Lee, S., Kim, S.-Y., Lee, B.-H., Kwon, T.-H., Park, R. W., & Kim, I. T. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402242 · Cited by 464 · see citing works
Sinha, P., Clements, V. K., & Ostrand‐Rosenberg, S. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.2.636 · Cited by 461 · see citing works
The E3 ligase Cbl-b and TAM receptors regulate cancer metastasis via natural killer cells
Paolino, M., Choidas, A., Wallner, S., Pranjic, B., Uribesalgo, I., Loeser, S., Jamieson, A. M., Langdon, W. Y., Ikeda, F., Fededa, J. P., et al. (2014) · Nature · doi:10.1038/nature12998 · Cited by 456 · see citing works
Stein, T., Morris, J. S., Davies, C. R., Weber-Hall, S., Duffy, M., Heath, V. J., Bell, A. K., Ferrier, R., Sandilands, G., & Gusterson, B. (2003) · Breast Cancer Research · doi:10.1186/bcr753 · Cited by 440 · see citing works
Activation of Rac1 by a Crk SH3-binding protein, DOCK180Preprint
Kiyokawa, E., Hashimoto, Y., Kobayashi, S., Sugimura, H., Kurata, T., & Matsuda, M. (1998) · Genes & Development · doi:10.1101/gad.12.21.3331 · Cited by 431 · see citing works
CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans
Reddien, P. W., & Horvitz, H. R. (2000) · Nature Cell Biology · doi:10.1038/35004000 · Cited by 414 · see citing works
Tzankov, A., Meier, C., Hirschmann, P., Went, P., Pileri, S. A., & Dirnhofer, S. (2008) · Haematologica · doi:10.3324/haematol.11702 · Cited by 412 · see citing works
Lyons, T. R., O’Brien, J., Borges, V. F., Conklin, M. W., Keely, P. J., Eliceiri, K. W., Marusyk, A., Tan, A. C., & Schedin, P. S. (2011) · Nature Medicine · doi:10.1038/nm.2416 · Cited by 381 · see citing works
Sisirak, V., Faget, J., Gobert, M., Goutagny, N., Vey, N., Treilleux, I., Renaudineau, S., Poyet, G., Labidi‐Galy, S. I., Goddard‐Léon, S., et al. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-3468 · Cited by 346 · see citing works
Expansion of spleen myeloid suppressor cells represses NK cell cytotoxicity in tumor-bearing host
Liu, C., Yu, S., Kappes, J. C., Wang, J., Grizzle, W. E., Zinn, K. R., & Zhang, H. (2007) · Blood · doi:10.1182/blood-2006-09-046201 · Cited by 335 · see citing works
DOCK180, a Major CRK-Binding Protein, Alters Cell Morphology upon Translocation to the Cell Membrane
Hasegawa, H., Kiyokawa, E., Tanaka, S., Nagashima, K., Gotoh, N., Shibuya, M., Kurata, T., & Matsuda, M. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.4.1770 · Cited by 335 · see citing works
DeKruyff, R. H., Bu, X., Ballesteros, Á., Santiago, C. A., Chim, Y.-L., Lee, H., Karisola, P., Pichavant, M., Kaplan, G. G., Umetsu, D. T., et al. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903059 · Cited by 331 · see citing works
Clarkson, R. W. E., Wayland, M. T., Lee, J., Freeman, T. C., & Watson, C. J. (2003) · Breast Cancer Research · doi:10.1186/bcr754 · Cited by 329 · see citing works
Camenisch, T. D., Koller, B. H., Earp, H. S., & Matsushima, G. K. (1999) · PubMed · Cited by 321 · see citing works
Sinha, P., Clements, V. K., & Ostrand‐Rosenberg, S. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-0045 · Cited by 317 · see citing works
Yang, 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
Luciani, M. F., & Chimini, G. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00353.x · Cited by 295 · see citing works
O’Brien, J., Lyons, T. R., Monks, J., Lucia, M. S., Wilson, R. S., Hines, L. M., Man, Y.-G., Borges, V. F., & Schedin, P. S. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090735 · Cited by 288 · see citing works
The final step in programmed cell death: phagocytes carry apoptotic cells to the grave
deCathelineau, A. M., & Henson, P. M. (2003) · Essays in Biochemistry · doi:10.1042/bse0390105 · Cited by 282 · see citing works
Apoptosis in the terminal endbud of the murine mammary gland: a mechanism of ductal morphogenesis
Humphreys, R. C., Krajewska, M., Krnacik, S., Jæger, R., Weiher, H., Krajewski, S., Reed, J. C., & Rosen, J. M. (1996) · Development · doi:10.1242/dev.122.12.4013 · Cited by 260 · see citing works
Tallerico, R., Todaro, M., Franco, S. D., Maccalli, C., Garofalo, C., Sottile, R., Palmieri, C., Tirinato, L., Pangigadde, P., Rocca, R. L., et al. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1201542 · Cited by 251 · see citing works
Ishimoto, Y., Ohashi, K., Mizuno, K., & Nakano, T. (2000) · Journal of Biochemistry (Tokyo) · doi:10.1093/oxfordjournals.jbchem.a022622 · Cited by 248 · see citing works
Callihan, E., Gao, D., Jindal, S., Lyons, T. R., Manthey, E., Edgerton, S. M., Urquhart, A., Schedin, P. S., & Borges, V. F. (2013) · Breast Cancer Research and Treatment · doi:10.1007/s10549-013-2437-x · Cited by 246 · see citing works
Remodeling of the Mammary Microenvironment after Lactation Promotes Breast Tumor Cell Metastasis
McDaniel, S. M., Rumer, K. K., Biroc, S. L., Metz, R. P., Singh, M., Porter, W. W., & Schedin, P. S. (2006) · American Journal Of Pathology · doi:10.2353/ajpath.2006.050677 · Cited by 234 · see citing works
Mechanisms and consequences of efferocytosis in advanced atherosclerosis
Thorp, E., & Tabas, I. (2009) · Journal of Leukocyte Biology · doi:10.1189/jlb.0209115 · Cited by 231 · see citing works
Akakura, S., Singh, S., Spataro, M., Akakura, R., Kim, J., Albert, M. L., & Birge, R. B. (2003) · Experimental Cell Research · doi:10.1016/j.yexcr.2003.09.011 · Cited by 229 · see citing works
Targeting Axl and Mer Kinases in Cancer
Verma, A. R., Warner, S. L., Vankayalapati, H., Bearss, D. J., & Sharma, S. (2011) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-11-0116 · Cited by 226 · see citing works
Santiago, C. A., Ballesteros, Á., Martínez‐Muñoz, L., Mellado, M., Kaplan, G. G., Freeman, G. J., & Casasnovas, J. M. (2007) · Immunity · doi:10.1016/j.immuni.2007.11.008 · Cited by 224 · see citing works
Fas/CD95-Induced Chemokines Can Serve as “Find-Me” Signals for Apoptotic Cells
Cullen, S. P., Henry, C. M., Kearney, C. J., Logue, S. E., Feoktistova, M., Tynan, G. A., Lavelle, E. C., Leverkus, M., & Martin, S. J. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.01.025 · Cited by 222 · see citing works
Evidence That DOCK180 Up-regulates Signals from the CrkII-p130Cas Complex
Kiyokawa, E., Hashimoto, Y., Kurata, T., Sugimura, H., & Matsuda, M. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.38.24479 · Cited by 208 · see citing works
MerTK inhibition in tumor leukocytes decreases tumor growth and metastasis
Cook, R. S., Jacobsen, K. M., Wofford, A., DeRyckere, D., Stanford, J. C., Prieto, A. L., Redente, E. F., Sandahl, M. A., Hunter, D. M., Strunk, K. E., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci67655 · Cited by 186 · see citing works
Self-citationRodriguez‐Manzanet, R., Sanjuán, M. A. F., Wu, H. Y., Quintana, F. J., Xiao, S., Anderson, A. C., Weiner, H. L., Green, D. R., & Kuchroo, V. K. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910359107 · Cited by 182 · see citing works
Soki, F. N., Koh, A. J., Jones, J., Kim, Y. W., Dai, J., Keller, E. T., Pienta, K. J., Atabai, K., Roca, H., & McCauley, L. K. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.571620 · Cited by 173 · see citing works
UNC2025 , a Potent and Orally Bioavailable MER/FLT3 Dual Inhibitor
Zhang, W., DeRyckere, D., Hunter, D. M., Liu, J., Stashko, M. A., Minson, K. A., Cummings, C. T., Lee, M., Glaros, T., Newton, D. L., et al. (2014) · Journal of Medicinal Chemistry · doi:10.1021/jm500749d · Cited by 172 · see citing works
Aziz, M., Jacob, A., Matsuda, A., & Wang, P. (2011) · APOPTOSIS · doi:10.1007/s10495-011-0630-0 · Cited by 163 · see citing works
Efferocytosis produces a prometastatic landscape during postpartum mammary gland involution
Stanford, J. C., Young, C. D., Hicks, D. J., Owens, P., Williams, A., Vaught, D., Morrison, M. M., Lim, J., Williams, M. M., Brantley‐Sieders, D. M., et al. (2014) · Journal of Clinical Investigation · doi:10.1172/jci76375 · Cited by 160 · see citing works
Self-citationMonks, J., Smith-Steinhart, C., Kruk, E. R., Fadok, V. A., & Henson, P. M. (2007) · Biology of Reproduction · doi:10.1095/biolreprod.107.065045 · Cited by 158 · see citing works
Microenvironment of the Involuting Mammary Gland Mediates Mammary Cancer Progression
Schedin, P. S., O’Brien, J., Rudolph, M. C., Stein, T., & Borges, V. F. (2007) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-007-9039-3 · Cited by 157 · see citing works
NAKANO, T., KAWAMOTO, K., Kishino, J., Nomura, K., Higashino, K., & Arita, H. (1997) · Biochemical Journal · doi:10.1042/bj3230387 · Cited by 154 · see citing works
Natural killer cells kill human melanoma cells with characteristics of cancer stem cells
Pietra, G., Manzini, C., Vitale, M., Balsamo, M. L., Ognio, E., Boitano, M., Queirolo, P., Moretta, L., & Mingari, M. C. (2009) · International Immunology · doi:10.1093/intimm/dxp047 · Cited by 148 · see citing works
Martinson, H. A., Jindal, S., Durand‐Rougely, C., Borges, V. F., & Schedin, P. S. (2014) · International Journal of Cancer · doi:10.1002/ijc.29181 · Cited by 145 · see citing works
Cyclooxygenase-2–dependent lymphangiogenesis promotes nodal metastasis of postpartum breast cancer
Lyons, T. R., Borges, V. F., Betts, C. B., Guo, Q., Kapoor, P., Martinson, H. A., Jindal, S., & Schedin, P. S. (2014) · Journal of Clinical Investigation · doi:10.1172/jci73777 · Cited by 135 · see citing works
Nonsteroidal Anti-Inflammatory Drug Use and Breast Cancer Risk by Stage and Hormone Receptor Status
Marshall, S. F., Bernstein, L., Anton‐Culver, H., Deapen, D., Horn‐Ross, P. L., Mohrenweiser, H. W., Peel, D. A., Pinder, R., Purdie, D. M., Reynolds, P., et al. (2005) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/dji140 · Cited by 133 · see citing works
Efferocytosis and Lung Disease
McCubbrey, A. L., & Curtis, J. L. (2013) · CHEST Journal · doi:10.1378/chest.12-2413 · Cited by 130 · see citing works
Sinha, P., Clements, V. K., Miller, S., & Ostrand‐Rosenberg, S. (2005) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-005-0703-4 · Cited by 126 · see citing works
Borisenko, G. G., Matsura, T., Liu, S., Tyurin, V. A., Jiang, J., Serinkan, F. B., & Kagan, V. E. (2003) · Archives of Biochemistry and Biophysics · doi:10.1016/s0003-9861(03)00083-3 · Cited by 125 · see citing works
Induced and natural regulatory T cells in human cancer
Whiteside, T. L., Schuler, P. J., & Schilling, B. (2012) · Expert Opinion on Biological Therapy · doi:10.1517/14712598.2012.707184 · Cited by 124 · see citing works
Roles of the Innate Immune System in Mammary Gland Remodeling During Involution
Atabai, K., Sheppard, D., & Werb, Z. (2007) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-007-9036-6 · Cited by 123 · see citing works
An AXL/LRP-1/RANBP9 complex mediates DC efferocytosis and antigen cross-presentation in vivo
Subramanian, M., Hayes, C. D., Thome, J. J. C., Thorp, E. B., Matsushima, G. K., Herz, J., Färber, D. L., Liu, K., Lakshmana, M. K., & Tabas, I. A. (2014) · Journal of Clinical Investigation · doi:10.1172/jci72051 · Cited by 123 · see citing works
IL-2–dependent adaptive control of NK cell homeostasis
Gasteiger, G., Hemmers, S., Bos, P. D., Sun, J. C.-Y., & Rudensky, A. Y. (2013) · The Journal of Experimental Medicine · doi:10.1084/jem.20122571 · Cited by 123 · see citing works
Frisdal, É., Lesnik, P., Olivier, M., Robillard, P., Chapman, M. J., Huby, T., Guérin, M., & Goff, W. L. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.264325 · Cited by 114 · see citing works
Bardia, A., Olson, J. E., Vachon, C. M., Lazovich, D., Vierkant, R. A., Wang, A. H., Limburg, P. J., Anderson, K. E., & Cerhan, J. R. (2010) · Breast Cancer Research and Treatment · doi:10.1007/s10549-010-1074-x · Cited by 111 · see citing works
Faupel‐Badger, J. M., Arcaro, K. F., Balkam, J. J., Eliassen, A. H., Hassiotou, F., Lebrilla, C. B., Michels, K. B., Palmer, J. R., Schedin, P. S., Stuebe, A. M., et al. (2012) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djs505 · Cited by 110 · see citing works
Association between NSAIDs use and breast cancer risk: a systematic review and meta-analysis
Zhao, Y., Zhu, S., Li, X., Wang, F., Hu, F., Li, D., Zhang, W., & Li, X. (2008) · Breast Cancer Research and Treatment · doi:10.1007/s10549-008-0228-6 · Cited by 101 · see citing works
Nguyen, K.-Q. N., Tsou, W., Calarese, D. A., Kimani, S. G., Singh, S., Hsieh, S., Liu, Y., Lü, B., Wu, Y., Garforth, S., et al. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.570838 · Cited by 99 · see citing works
Jensen, H. K., Donskov, F. N., Nordsmark, M., Marcussen, N., & von der Maase, H. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-1296 · Cited by 96 · see citing works
The growing diversity and spectrum of action of myeloid‐derived suppressor cells
Mantovani, A. (2010) · European Journal of Immunology · doi:10.1002/eji.201041170 · Cited by 95 · see citing works
Wu, F., Li, J., Jang, C., Wang, J., & Xiong, J. (2014) · PubMed Central · Cited by 85 · see citing works
Sandahl, M. A., Hunter, D. M., Strunk, K. E., Earp, H. S., & Cook, R. S. (2010) · BMC Developmental Biology · doi:10.1186/1471-213x-10-122 · Cited by 79 · see citing works
Self-citationPark, S., Kim, S., Jung, M.-Y., Bae, D.-J., & Kim, I. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.01993-07 · Cited by 78 · see citing works
Christoph, S., DeRyckere, D., Schlegel, J., Frazer, J. K., Batchelor, L. A., Trakhimets, A. Y., Sather, S., Hunter, D. M., Cummings, C. T., Liu, J., et al. (2013) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-13-0040 · Cited by 72 · see citing works
Developmental windows of breast cancer risk provide opportunities for targeted chemoprevention
Martinson, H. A., Lyons, T. R., Giles, E. D., Borges, V. F., & Schedin, P. S. (2013) · Experimental Cell Research · doi:10.1016/j.yexcr.2013.04.018 · Cited by 62 · see citing works
O'Brien, J., Hansen, K. C., Barkan, D., Green, J., & Schedin, P. (2011) · International Journal of Developmental Biology · doi:10.1387/ijdb.113379jo · Cited by 60 · see citing works
Brasky, T. M., Bonner, M. R., Moysich, K. B., Ambrosone, C. B., Nie, J., Tao, M. H., Edge, S. B., Kallakury, B., Marian, C., Goerlitz, D. S., et al. (2011) · Cancer Causes & Control · doi:10.1007/s10552-011-9769-9 · Cited by 57 · see citing works
Discovery of Mer Specific Tyrosine Kinase Inhibitors for the Treatment and Prevention of Thrombosis
Zhang, W., McIver, A. L., Stashko, M. A., DeRyckere, D., Branchford, B. R., Hunter, D. M., Kireev, D., Miley, M. J., Norris-Drouin, J. L., Stewart, W. M., et al. (2013) · Journal of Medicinal Chemistry · doi:10.1021/jm4013888 · Cited by 53 · see citing works
Apoptosis in the Estrous and Menstrual Cycles
Andres, A., & Strange, R. (1999) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1023/a:1018737510695 · Cited by 53 · see citing works
Clearance of apoptotic β-cells is reduced in neonatal autoimmune diabetes-prone rats
O’Brien, B. A., Fieldus, W. E., Field, C. J., & Finegood, D. T. (2002) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400973 · Cited by 50 · see citing works
Mani, O., Körner, M., Sørensen, M. T., Sejrsen, K., Wotzkow, C., Ontsouka, C. E., Friis, R. R., Bruckmaier, R. M., & Albrecht, C. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00723.2009 · Cited by 48 · see citing works
Ramirez, R. A., Lee, A. S., Schedin, P. S., Russell, J. S., & Masso‐Welch, P. A. (2012) · Developmental Dynamics · doi:10.1002/dvdy.23778 · Cited by 28 · see citing works
O’Brien, J., Fornetti, J., & Schedin, P. S. (2010) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-010-9185-x · Cited by 22 · see citing works
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Myers, K. V., Amend, S. R., & Pienta, K. J. (2019) · Molecular Cancer · doi:10.1186/s12943-019-1022-2 · Cited by 482 · see citing works
Drugging the efferocytosis process: concepts and opportunities
Mehrotra, P., & Ravichandran, K. S. (2022) · Nature Reviews Drug Discovery · doi:10.1038/s41573-022-00470-y · Cited by 459 · see citing works
Macrophages at the interface of the co-evolving cancer ecosystem
Kloosterman, D. J., & Akkari, L. (2023) · Cell · doi:10.1016/j.cell.2023.02.020 · Cited by 436 · see citing works
The Multifaceted Role of STAT3 in Mammary Gland Involution and Breast Cancer
Hughes, K., & Watson, C. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19061695 · Cited by 69 · see citing works
Wu, C., Tan, X., Hu, X., Zhou, M., Yan, J., & Ding, C. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1900930 · Cited by 69 · see citing works
The complex roles of efferocytosis in cancer development, metastasis, and treatment
Tajbakhsh, A., Gheibi hayat, S. M., Movahedpour, A., Savardashtaki, A., Loveless, R., Barreto, G. E., Teng, Y., & Sahebkar, A. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.111776 · Cited by 64 · see citing works
Macrophage variants in laboratory research: most are well done, but some are RAW
Herb, M., Schatz, V., Hadrian, K., Hos, D., Holoborodko, B., Jantsch, J., & Brigo, N. (2024) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2024.1457323 · Cited by 63 · see citing works
Asare, P. F., Roscioli, E., Hurtado, P. R., Tran, H. B., Mah, C. Y., & Hodge, S. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.01298 · Cited by 50 · see citing works
Kim, H. J., Yang, K., Kim, K., Lee, Y., Lee, S., Ahn, S. Y., Ahn, Y., & Kang, J. L. (2022) · Cellular & Molecular Immunology · doi:10.1038/s41423-022-00930-w · Cited by 50 · see citing works
Kim, Y.-B., Ahn, Y.-H., Jung, J.-H., Lee, Y.-J., Lee, J.-H., & Kang, J. L. (2019) · Cellular & Molecular Immunology · doi:10.1038/s41423-019-0209-1 · Cited by 45 · see citing works
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Lin, D., Kang, X., Shen, L. H., Tu, S., Lenahan, C., Chen, Y., Wang, X., & Shao, A. (2020) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2020.04.010 · Cited by 44 · see citing works
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Gadiyar, V., Lahey, K. C., Calianese, D. C., Devoe, C., Mehta, D., Bono, K. R., Desind, S. Z., Davra, V., & Birge, R. B. (2020) · Cells · doi:10.3390/cells9102207 · Cited by 44 · see citing works
Mann, V., Sundaresan, A., & Shishodia, S. (2024) · Biology · doi:10.3390/biology13040241 · Cited by 41 · see citing works
Mertk: An emerging target in cancer biology and immuno-oncology
Lahey, K. C., Gadiyar, V., Hill, A. A., Desind, S. Z., Wang, Z., Davra, V., Patel, R., Zaman, A., Calianese, D. C., & Birge, R. B. (2022) · International review of cytology · doi:10.1016/bs.ircmb.2022.04.004 · Cited by 32 · see citing works
Role of Apoptotic Cell Clearance in Pneumonia and Inflammatory Lung Disease
Zheng, D. J., Taka, M. A., & Heit, B. (2021) · Pathogens · doi:10.3390/pathogens10020134 · Cited by 32 · see citing works
Efferocytosis of vascular cells in cardiovascular disease
Cabrera, J. T. O., & Makino, A. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107919 · Cited by 31 · see citing works
Lang, C., Roy, S., Wang, Y., Graves, D. K., Xu, Y., Serezani, C. H., Korrer, M. J., & Kim, Y. J. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.993771 · Cited by 24 · see citing works
Beizavi, Z., Hayat, S. M. G., Moghadasian, H., Zare, H., Yeganeh, B. S., Askari, H., Vakili, S., Tajbakhsh, A., & Savardashtaki, A. (2021) · Molecular Biology Reports · doi:10.1007/s11033-021-06547-y · Cited by 23 · see citing works
Liu, T., Li, C. R., Zhang, J., Hu, H., & Li, C. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1237350 · Cited by 20 · see citing works
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Liu, Z., Li, Y., Ren, Y., Chen, J., Weng, S., Zhou, Z., Luo, P., Cheng, Q., Xu, H., Ba, Y., et al. (2025) · Aging Cell · doi:10.1111/acel.14467 · Cited by 19 · see citing works
Huang, H., Jiang, J., Chen, R., Lin, Y., Chen, H., & Ling, Q. (2022) · Liver International · doi:10.1111/liv.15380 · Cited by 19 · see citing works
Mendoza‐Reinoso, V., Schnepp, P. M., Baek, D. Y., Rubin, J. R., Schipani, E., Keller, E. T., McCauley, L. K., & Roca, H. (2022) · Cells · doi:10.3390/cells11233712 · Cited by 18 · see citing works
Zheng, X., Liu, H., Zhang, L., Liu, X., Zhong, X., Zhou, C., Hu, T., Wu, X., Hu, J., Lian, L., et al. (2018) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjy133 · Cited by 18 · see citing works
The Role of Antigen Presentation in Tumor-Associated Macrophages
Stopforth, R. J., & Ward, E. S. (2020) · Critical Reviews in Immunology · doi:10.1615/critrevimmunol.2020034910 · Cited by 16 · see citing works
Kim, S.-Y., Yang, K., Kim, K., Kim, H. J., Kim, D. Y., Chae, J., Ahn, Y., & Kang, J. L. (2025) · Cell Communication and Signaling · doi:10.1186/s12964-025-02094-2 · Cited by 13 · see citing works
Zhang, Y., Nie, R., Feng, Z.-Y., Fan, M., Shen, Z., Zhang, X., Zhang, Q., Zou, C., Zhang, J., Huang, K., et al. (2025) · Bioactive Materials · doi:10.1016/j.bioactmat.2025.05.026 · Cited by 13 · see citing works
Snyder, C. M., & Gill, S. I. (2023) · Immunological Reviews · doi:10.1111/imr.13231 · Cited by 12 · see citing works
Quantification of Efferocytosis by Single-cell Fluorescence Microscopy
Taruc, K., Yin, C., Wootton, D. G., & Heit, B. (2018) · Journal of Visualized Experiments · doi:10.3791/58149 · Cited by 11 · see citing works
Bumm, C. V., Folwaczny, M., & Wölfle, U. C. (2020) · Oral and Maxillofacial Surgery · doi:10.1007/s10006-020-00851-w · Cited by 9 · see citing works
Cholesterol efflux protein, ABCA1, supports anticancer functions of myeloid immune cells
Bendre, S. V., Wang, Y., Hajyousif, B., K C, R., Bhogale, S. G., Pradeep, D., Krawczynska, N., Schane, C. P., Weisser, E., Singh, A., et al. (2026) · Science Advances · doi:10.1126/sciadv.adx5490 · Cited by 8 · see citing works
Xu, K., Liu, Y. S., Luo, H., & Wang, T. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1218244 · Cited by 8 · see citing works
Carcinogenesis-relevant biological events in the pathophysiology of the efferocytosis phenomenon
Sarode, G. S., Sarode, S. C., Maniyar, N., Sharma, N. K., & Patil, S. (2017) · Oncology Reviews · doi:10.4081/oncol.2017.343 · Cited by 8 · see citing works
Silini, A. R., Ramuta, T. Ž., Pires, A. S., Banerjee, A., Dubus, M., Gindraux, F., Kerdjoudj, H., Mačiulaitis, J., Weidinger, A., Wolbank, S., et al. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.958669 · Cited by 6 · see citing works
Death as rebirth: how efferocytosis drives tissue repair and disease treatment
Duan, X., Han, S., Bian, Y., Yuan, Y., Shen, J., Dai, Y., Mi, J., & Wang, Z. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1712547 · Cited by 3 · see citing works
Goodin, D. A., & Frieboes, H. B. (2022) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2022.111383 · Cited by 3 · see citing works
Zhou, C., Gan, X., Sun, S., Wang, L., Zhang, Y., & Zhang, J. (2023) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2023.101540 · Cited by 2 · see citing works
Nguyen, Q. A., Wang, H., Verghese, E., Iscaro, J., Steinfort, D., McQualter, J. L., & Bozinovski, S. (2025) · Clinical and Experimental Medicine · doi:10.1007/s10238-025-01881-y · Cited by 1 · see citing works
Mendoza‐Reinoso, V., Schnepp, P. M., Baek, D. Y., Rubin, J. R., Schipani, E., Keller, E. T., McCauley, L. K., & Roca, H. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.02.458687
Immune Regulation of Tumors in Bone
Ricci, B., Zimmerman, S. M., Wang, W., & Faccio, R. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.11247-4
Chamberland, M. M., Farrell, B. M., & Yeh, J. T. ‐. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.06.21.497076
Park, J. Y., McCaw, T. R., Dao, H., Donahue, T. R., Crompton, J., Vlashi, E., & Girgis, M. D. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.12.669943
Shi, B., Deng, M., Ma, J., Chen, C., Peng, A., Zhu, A., Yang, R., Jin, Z., Zhu, J., Zhang, M., et al. (2025) · Mediators of Inflammation · doi:10.1155/mi/8710699
Li, X., Zhang, Y., Wei, X., & Huang, R. (2026) · Annals of Hematology · doi:10.1007/s00277-026-07044-7
Role of Macrophage Efferocytosis in Cardiovascular Homeostasis and Disease
Lin, H., Zhu, X., Sun, Y., Yang, Y., Fan, A., Yang, K., Gao, Z., Ma, C., Fan, G., & Li, L. (2026) · Frontiers in Bioscience-Landmark · doi:10.31083/fbl49006
- Authors
- Vaught, D., Stanford, J. C., & Cook, R. S.
- Affiliations
- Vanderbilt University (US)
- Venue
- Cancer Cell & Microenvironment
- Publisher
- Smart Science and Technology, LLC
- Published
- 2015-03-18
- Volume
- 2
- Issue
- 1
- ISSN
- 2331-091X (ISSN-L)
- 2331-0928
- PMC
- PMC5734109
- OpenAlex
- W1666037483
- Cited by
- 44
- References
- 114
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 2 · 2023: 5 · 2022: 9 · 2021: 5 · 2020: 5 · 2019: 4 · 2018: 3 · 2017: 1
- FWCI
- 0.66
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cancer Cell & Microenvironment (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (R01CA143126, T32CA009592)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- efferocytosis, tumor microenvironment, apoptosis, phagocytes, immunosuppression, metastasis, tumor cell motility, cancer therapy targets
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