Immune system: a double-edged sword in cancer
Abstract
Objective The objective of the review is to examine the role of innate and adaptive immune cells in cancer.Introduction Immune system functions as a host defensive mechanism protecting against invading pathogens and transformed cells, including cancer. However, a body of research carried out over the last few decades has disclosed the unexpected role of immune system in fostering the tumor growth.Methods A computer-based online search was performed in the PubMed, Scopus and Web of Science databases for articles published, concerning natural killer (NK) cells, Macrophages, CD4+ and CD8+ T cells with relevance to cancer. After finding relevant articles within these search limits, a manual search was conducted through the references from these articles.Results and conclusions This review summarizes the role of immune system in Immunosurveillance and Immunoediting. It then focused mainly on role of macrophages, regulatory T cells (Treg), TH17 cells and on the immunosuppressive mechanisms, which facilitate immune evasion of tumor cells. Our results shows that, immune cells, such as CD8+ cytotoxic T lymphocytes (CTL), CD4+ T helper (TH)1 cells and NK cells along with their characteristic cytokine interferon (IFN)-γ, function as major antitumor effector cells. Whereas CD4+TH2 cells, myeloid-derived suppressor cells (MDSCs) and their derived cytokines function as dominant tumor-promoting forces. In contrast to these cells, macrophages, Treg, and TH17 cells show a dual effect in cancer. Thus, it appears that most components of the immune system are potentially endowed with dual functions i.e., promoting tumor development on the one hand and restraining tumor development on the other and hence immune system can be considered as a double-edged sword in cancer.
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?
The decrease of M2-like macrophages favors lung metastasis inhibition due to a lack of tumor-angiogenesis factors such as VEGF, EGF, FGF, and MMP-2 and MMP-9 which promote tumor angiogenesis and metastasis.
“Furthermore, the decrease of M2-like macrophages favors lung metastasis inhibition due to a lack of tumor-angiogenesis factors such as vascular endothelial growth factor (VEGF), epidermal growth factor (EGF) and fibroblast growth factor (FGF), and matrix metalloproteases (MMP-2 and MMP-9) which promote tumor angiogenesis, and metastasis (44).”
From mRNA vaccine with unmodified uridine induces robust type I interferon-dependent anti-tumor immunity in a melanoma model (2022) · cites this paper as [44]
Cites
The chemokine system in diverse forms of macrophage activation and polarization
MANTOVANI, A., SICA, A., SOZZANI, S., ALLAVENA, P., VECCHI, A., & LOCATI, M. (2004) · Trends in Immunology · doi:10.1016/j.it.2004.09.015 · Cited by 6,534 · see citing works
Park, J., Adoro, S., Guinter, T. I., Erman, B., Alag, A., Catálfamo, M., Kimura, M. Y., Cui, Y., Lucas, P. J., Gress, R. E., et al. (2010) · Nature Immunology · doi:10.1038/ni.1840 · Cited by 5,835 · see citing works
Sakaguchi, S., Sakaguchi, N., Asano, M., Itoh, M., & Toda, M. (1995) · The Journal of Immunology · doi:10.4049/jimmunol.155.3.1151 · Cited by 5,608 · see citing works
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
Cancer immunoediting: from immunosurveillance to tumor escape
Dunn, G. P., Bruce, A. T., Ikeda, H., Old, L. J., & Schreiber, R. D. (2002) · Nature Immunology · doi:10.1038/ni1102-991 · Cited by 5,393 · 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
Ivanov, I. I., McKenzie, B. S., Zhou, L., Tadokoro, C. E., Lepelley, A., Lafaille, J. J., Cua, D. J., & Littman, D. R. (2006) · Cell · doi:10.1016/j.cell.2006.07.035 · Cited by 5,145 · see citing works
Harrington, L. E., Hatton, R. D., Mangan, P. R., Turner, H., Murphy, T. L., Murphy, K. M., & Weaver, C. T. (2005) · Nature Immunology · doi:10.1038/ni1254 · Cited by 4,742 · 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
The Three Es of Cancer Immunoediting
Dunn, G. P., Old, L. J., & Schreiber, R. D. (2004) · Annual Review of Immunology · doi:10.1146/annurev.immunol.22.012703.104803 · Cited by 3,087 · see citing works
The Immunobiology of Cancer Immunosurveillance and Immunoediting
Dunn, G. P., Old, L. J., & Schreiber, R. D. (2004) · Immunity · doi:10.1016/j.immuni.2004.07.017 · Cited by 3,036 · see citing works
Alternative Activation of Macrophages: An Immunologic Functional Perspective
Martinez, F. O., Helming, L., & Gordon, S. (2009) · Annual Review of Immunology · doi:10.1146/annurev.immunol.021908.132532 · Cited by 2,745 · see citing works
Deaglio, S., Dwyer, K. M., Gao, W., Friedman, D. J., Usheva, A., Erat, A., Chen, J., Enjyoji, K., Linden, J. M., Oukka, M., et al. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20062512 · Cited by 2,478 · see citing works
Uyttenhove, C., Pilotte, L., Théate, I., Stroobant, V., Colau, D., Parmentier, N., Boon, T., & Van den Eynde, B. J. (2003) · Nature Medicine · doi:10.1038/nm934 · Cited by 2,305 · see citing works
The inhibitory cytokine IL-35 contributes to regulatory T-cell function
Collison, L., Workman, C., Kuo, T. T., Boyd, K., Wang, Y., Vignali, K. M., Cross, R., Sehy, D., Blumberg, R., & Vignali, D. (2007) · Nature · doi:10.1038/nature06306 · Cited by 2,152 · see citing works
Natural Innate and Adaptive Immunity to Cancer
Vesely, M. D., Kershaw, M. H., Schreiber, R. D., & Smyth, M. J. (2011) · Annual Review of Immunology · doi:10.1146/annurev-immunol-031210-101324 · Cited by 2,095 · see citing works
Plasticity of CD4+ T Cell Lineage Differentiation
Zhou, L., Chong, M. M. W., & Littman, D. R. (2009) · Immunity · doi:10.1016/j.immuni.2009.05.001 · Cited by 1,551 · see citing works
Swann, J. B., & Smyth, M. J. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31405 · Cited by 1,469 · see citing works
Generation of pathogenic TH17 cells in the absence of TGF-β signalling
Ghoreschi, K., Laurence, A., Yang, X.-P., Tato, C. M., McGeachy, M. J., Konkel, J. E., Ramos, H. L., Wei, L., Davidson, T. S., Bouladoux, N., et al. (2010) · Nature · doi:10.1038/nature09447 · Cited by 1,388 · see citing works
Pandiyan, P., Zheng, L., Ishihara, S., Reed, J., & Lenardo, M. J. (2007) · Nature Immunology · doi:10.1038/ni1536 · Cited by 1,288 · see citing works
Borsellino, G., Kleinewietfeld, M., Mitri, D. D., Sternjak, A., Diamantini, A., Giometto, R., Höpner, S., Centonze, D., Bernardi, G., Dell’Acqua, M. L., et al. (2007) · Blood · doi:10.1182/blood-2006-12-064527 · Cited by 1,287 · 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
Interleukin‐10‐secreting type 1 regulatory T cells in rodents and humans
Roncarolo, M. G., Gregori, S., Battaglia, M., Bacchetta, R., Fleischhauer, K., & Levings, M. K. (2006) · Immunological Reviews · doi:10.1111/j.0105-2896.2006.00420.x · Cited by 1,174 · see citing works
Tosolini, M., Kirilovsky, A., Mlecnik, B., Fredriksen, T., Mauger, S., Bindea, G., Berger, A., Bruneval, P., Fridman, W.-H., Pagès, F., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-2907 · Cited by 1,146 · 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
Tesmer, L. A., Lundy, S. K., Sarkar, S., & Fox, D. A. (2008) · Immunological Reviews · doi:10.1111/j.1600-065x.2008.00628.x · Cited by 1,097 · see citing works
Indoleamine 2,3-dioxygenase and tumor-induced tolerance
Munn, D. H., & Mellor, A. L. (2007) · Journal of Clinical Investigation · doi:10.1172/jci31178 · Cited by 1,074 · see citing works
Late Developmental Plasticity in the T Helper 17 Lineage
Lee, Y. K., Turner, H., Maynard, C. L., Oliver, J. R., Chen, D., Elson, C. O., & Weaver, C. T. (2009) · Immunity · doi:10.1016/j.immuni.2008.11.005 · Cited by 1,053 · see citing works
Granzyme B and Perforin Are Important for Regulatory T Cell-Mediated Suppression of Tumor Clearance
Cao, X., Cai, S. F., Fehniger, T. A., Song, J., Collins, L. I., Piwnica-Worms, D. R., & Ley, T. J. (2007) · Immunity · doi:10.1016/j.immuni.2007.08.014 · Cited by 1,038 · see citing works
Macrophages 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
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
IL-21 and TGF-β are required for differentiation of human TH17 cells
Yang, L., Anderson, D. E., Baecher‐Allan, C., Hastings, W. D., Bettelli, E., Oukka, M., Kuchroo, V. K., & Hafler, D. A. (2008) · Nature · doi:10.1038/nature07021 · Cited by 926 · see citing works
Hiraoka, N., Onozato, K., Kosuge, T., & Hirohashi, S. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-0369 · Cited by 831 · 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
Roncarolo, M. G., Bacchetta, R., Bordignon, C., Narula, S. K., & Levings, M. K. (2001) · Immunological Reviews · doi:10.1034/j.1600-065x.2001.1820105.x · Cited by 814 · see citing works
Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells
Gallina, G., Dolcetti, L., Serafini, P., Santo, C. D., Marigo, I., Colombo, M. P., Basso, G., Brombacher, F., Borrello, I., Zanovello, P., et al. (2006) · Journal of Clinical Investigation · doi:10.1172/jci28828 · Cited by 792 · see citing works
T Cell-Dependent B Cell Activation
Parker, D. C. (1993) · Annual Review of Immunology · doi:10.1146/annurev.iy.11.040193.001555 · Cited by 739 · see citing works
Human CD25highFoxp3pos regulatory T cells differentiate into IL-17–producing cells
Koenen, H. J. P. M., Smeets, R. L., Vink, P. M., van Rijssen, E., Boots, A. M. H., & Joosten, I. (2008) · Blood · doi:10.1182/blood-2008-01-133967 · Cited by 735 · see citing works
Epigenetic control of T-helper-cell differentiation
Wilson, C. B., Rowell, E. A., & Sekimata, M. (2009) · Nature reviews. Immunology · doi:10.1038/nri2487 · Cited by 678 · see citing works
Tan, W., Zhang, W., Strasner, A., Grivennikov, S. I., Cheng, J. Q., Hoffman, R. M., & Karin, M. (2011) · Nature · doi:10.1038/nature09707 · Cited by 647 · see citing works
Prognostic Value of Tumor-Infiltrating CD4+ T-Cell Subpopulations in Head and Neck Cancers
Badoual, C., Hans, S., Rodriguez, J., Peyrard, S., Klein, C., Agueznay, N. E. H., Mosseri, V., Laccourreye, O., Bruneval, P., Fridman, W. H., et al. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-1886 · Cited by 595 · see citing works
Zhang, J., Yan, J., Xu, J., Pang, X.-H., Chen, M.-S., Li, L., Wu, C. Y., Li, S., & Zheng, L. (2009) · Journal of Hepatology · doi:10.1016/j.jhep.2008.12.033 · Cited by 535 · see citing works
Silencing of Irf7 pathways in breast cancer cells promotes bone metastasis through immune escape
Bidwell, B. N., Slaney, C. Y., Withana, N. P., Forster, S., Cao, Y., Loi, S., Andrews, D., Mikeska, T., Mangan, N. E., Samarajiwa, S. A., et al. (2012) · Nature Medicine · doi:10.1038/nm.2830 · Cited by 487 · 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
Strauss, L., Bergmann, C., Szczepański, M. J., Gooding, W. E., Johnson, J. T., & Whiteside, T. L. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-0472 · Cited by 453 · see citing works
2011: the immune hallmarks of cancer
Cavallo, F., Giovanni, C. D., Nanni, P., Forni, G., & Lollini, P. (2011) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-010-0968-0 · Cited by 417 · see citing works
Role of macrophages in tumour progression
Siveen, K. S., & Kuttan, G. (2009) · Immunology Letters · doi:10.1016/j.imlet.2009.02.011 · Cited by 351 · see citing works
Tumor-associated macrophages: Effectors of angiogenesis and tumor progression
Coffelt, S. B., Hughes, R., & Lewis, C. E. (2009) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2009.02.004 · Cited by 350 · see citing works
Chalmin, F., Mignot, G., Bruchard, M., Chevriaux, A., Végran, F., Hichami, A., Ladoire, S., Derangère, V., Vincent, J., Masson, D., et al. (2012) · Immunity · doi:10.1016/j.immuni.2011.12.019 · Cited by 338 · see citing works
Frey, D. M., Droeser, R. A., Viehl, C. T., Zlobec, I., Lugli, A., Zingg, U., Oertli, D., Kettelhack, C., Terracciano, L., & Tornillo, L. (2009) · International Journal of Cancer · doi:10.1002/ijc.24989 · Cited by 335 · see citing works
Ladoire, S., Martin, F., & Ghiringhelli, F. (2011) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-011-1046-y · Cited by 331 · see citing works
FOXP3 Expression and Overall Survival in Breast Cancer
Merlo, A. C., Casalini, P., Carcangiu, M. L., Malventano, C., Triulzi, T., Ménard, S., Tagliabue, E., & Balsari, A. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2008.17.9036 · Cited by 301 · see citing works
What are regulatory T cells (Treg) regulating in cancer and why?
Whiteside, T. L. (2012) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2012.03.004 · Cited by 294 · see citing works
Alternatively activated macrophages in infection and autoimmunity
Fairweather, D., & Cihakova, D. (2009) · Journal of Autoimmunity · doi:10.1016/j.jaut.2009.09.012 · Cited by 290 · see citing works
Generation and regulation of human CD4 <sup>+</sup> IL-17-producing T cells in ovarian cancer
Miyahara, Y., Odunsi, K., Chen, W., Peng, G., Matsuzaki, J., & Wang, R.-F. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710686105 · Cited by 279 · see citing works
Jordanova, E. S., Gorter, A., Ayachi, O., Prins, F., Durrant, L. G., Kenter, G. G., van der Burg, S. H., & Fleuren, G. J. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-4554 · Cited by 233 · see citing works
Shin, M. S., Kim, H. S., Lee, S. H., et al. (2001) · PubMed · Cited by 230 · see citing works
Toward the identification of a tolerogenic signature in IDO-competent dendritic cells
Orabona, C., Puccetti, P., Vacca, C., Bicciato, S., Luchini, A., Fallarino, F., Bianchi, R., Velardi, E., Perruccio, K., Velardi, A., et al. (2005) · Blood · doi:10.1182/blood-2005-10-4077 · Cited by 186 · see citing works
Natural killer cells: role in local tumor growth and metastasis
Jacobs, N., Langers, Renoux, Thiry, & Delvenne (2012) · Biologics · doi:10.2147/btt.s23976 · Cited by 167 · see citing works
MHC class I down-regulation: tumour escape from immune surveillance? (Review)
Bubenik, J. (2004) · International Journal of Oncology · doi:10.3892/ijo.25.2.487 · Cited by 167 · see citing works
Valmori, D., Raffin, C., Raimbaud, I., & Ayyoub, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1008247107 · Cited by 159 · see citing works
Mandapathil, M., Lang, S., Gorelik, E., et al. (2009) · Journal of Immunological Methods · doi:10.1016/j.jim.2009.05.004 · Cited by 154 · see citing works
Bergmann, C., Strauss, L., Zeidler, R., Lang, S., & Whiteside, T. L. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-0767 · Cited by 153 · see citing works
Tumor-induced death of immune cells: its mechanisms and consequences
Whiteside, T. L. (2002) · Seminars in Cancer Biology · doi:10.1006/scbi.2001.0402 · Cited by 149 · see citing works
Different subsets of tumor infiltrating lymphocytes correlate with NPC progression in different ways
Zhang, Y.-L., Li, J., Mo, H., Qiu, F., Zheng, L., Qian, C.-N., & Zeng, Y.-X. (2010) · Molecular Cancer · doi:10.1186/1476-4598-9-4 · Cited by 149 · see citing works
He, S., Fei, M., Wu, Y., Zheng, D., Wan, D., Wang, L., & Li, D. (2011) · International Journal of Molecular Sciences · doi:10.3390/ijms12117424 · Cited by 141 · see citing works
An Update on Human Th1 and Th2 Cells
Romagnani, S., Parronchi, P., D’Elios, M. M., et al. (2009) · International Archives of Allergy and Immunology · doi:10.1159/000237532 · Cited by 139 · see citing works
Elpek, K. G., Lacelle, C., Singh, N. P., Yolcu, E. S., & Shirwan, H. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.11.6840 · Cited by 124 · see citing works
Oberle, N., Eberhardt, N., Falk, C. S., Krammer, P. H., & Suri‐Payer, E. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.6.3578 · Cited by 114 · see citing works
Functions of T-cell subsets and cytokines in mycobacterial infections.
Munk, M. E., & Emoto, M. (1995) · PubMed · Cited by 105 · see citing works
Antigenic drift as a mechanism for tumor evasion of destruction by cytolytic T lymphocytes
Bai, X., Liu, J., Ou, L., Zheng, P., & Liu, Y. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17656 · Cited by 105 · see citing works
Role of TGF-? in immune-evasion of cancer
Beck, C., Schreiber, H. W., & Rowley, D. A. (2001) · Microscopy Research and Technique · doi:10.1002/1097-0029(20010215)52:4 · Cited by 103 · see citing works
Lehmann, C., Zeis, M., Schmitz, N., et al. (2000) · Blood · doi:10.1182/blood.v96.2.594 · Cited by 102 · see citing works
Breast cancer and the immune system.
Standish, L. J., Sweet, E. S., Novack, J. P., Wenner, C. A., Bridge, C. A., Nelson, A., Martzen, M. R., & Torkelson, C. J. (2008) · PubMed · Cited by 98 · see citing works
Controversies on the role of Th17 in cancer: a TGF-β-dependent immunosuppressive activity?
Martin, F., Apétoh, L., & Ghiringhelli, F. (2012) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2012.09.007 · Cited by 90 · see citing works
Transformation of the microvascular system during multistage tumorigenesis
Ryschich, E., Schmidt, J., Hämmerling, G. J., Klar, E., & Ganß, R. (2002) · International Journal of Cancer · doi:10.1002/ijc.10074 · Cited by 85 · see citing works
Tumor Versus Tumor-Associated Macrophages: How Hot is the Link?
Guruvayoorappan, C. (2008) · Integrative Cancer Therapies · doi:10.1177/1534735408319060 · Cited by 83 · see citing works
OR.41. IL-21 and TGF-β are Required for Differentiation of Human Th17 Cells
Anderson, D., Yang, L., Baecher‐Allan, C., Bettelli, E., Oukka, M., Kuchroo, V. K., & Hafler, D. A. (2008) · Clinical Immunology · doi:10.1016/j.clim.2008.03.047 · Cited by 83 · see citing works
Ye, J., Su, X., Hsueh, E. C., Zhang, Y., Koenig, J. M., Hoft, D. F., & Peng, G. (2011) · European Journal of Immunology · doi:10.1002/eji.201040682 · Cited by 82 · see citing works
Dendritic Cells The Tumor Microenvironment and the Challenges for an Effective Antitumor Vaccination
Benencia, F., Sprague, L., McGinty, J. W., Pate, M., & Muccioli, M. (2012) · BioMed Research International · doi:10.1155/2012/425476 · Cited by 81 · see citing works
Dendritic cells in immunotherapy of established cancer: Roles of signals 1, 2, 3 and 4.
Kaliński, P. (2009) · PubMed · Cited by 73 · 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
Naturally Occurring Regulatory T Cells: Recent Insights in Health and Disease
Raimondi, G., Turner, M. S., Thomson, A. W., & Morel, P. A. (2007) · Critical Reviews in Immunology · doi:10.1615/critrevimmunol.v27.i1.50 · Cited by 72 · see citing works
Kawamura, K., Bahar, R., Natsume, W., et al. (2002) · Cancer Gene Therapy · doi:10.1038/sj.cgt.7700418 · Cited by 55 · see citing works
Spontaneous and induced primary oncogenesis in natural killer (nk)‐cell‐deficient beige mutant mice
Haliotis, T. P., Ball, J. K., Dexter, D. F., et al. (1985) · International Journal of Cancer · doi:10.1002/ijc.2910350414 · Cited by 54 · see citing works
Real, L. M., Jiménez, P., Kirkin, A. F., Serrano, A., Garcia-Lora, A. M., Cantón, J., Zeuthen, J., Garrido, F., & Ruiz‐Cabello, F. (2001) · Cancer Immunology Immunotherapy · doi:10.1007/s002620000154 · Cited by 48 · see citing works
The Roles of CD4+T Cells in Tumor Immunity
Lai, Y., Jeng, C., & Chen, S.-C. (2011) · ISRN Immunology · doi:10.5402/2011/497397 · Cited by 46 · see citing works
Zhang, X. M., & Xu, Q. (2001) · Melanoma Research · doi:10.1097/00008390-200112000-00002 · Cited by 37 · see citing works
Tumor microenvironments, the immune system and cancer survival.
Strausberg, R. L. (2005) · Genome biology · doi:10.1186/gb-2005-6-3-211 · Cited by 27 · see citing works
Kowalczyk, D. W. (2002) · Acta Biochimica Polonica · doi:10.18388/abp.2002_3787 · Cited by 25 · see citing works
Targeting Foxp3+ regulatory T cells-related immunosuppression for cancer immunotherapy.
Feng, L., & Wang, X. (2010) · PubMed · Cited by 22 · see citing works
Indoleamine 2,3-dioxygenase in tumor induced tolerance.
Liu, X.-Q., & Wang, X. (2009) · PubMed · Cited by 19 · see citing works
Obesity, Diabetes and Metabolic Syndrome Impact on Tumor Angiogenesis
Incio, J., & Soares, R. (2013) · CRC Press eBooks · doi:10.1201/b14842-13 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Functional Significance of CD57 Expression on Human NK Cells and Relevance to Disease
Nielsen, C. M., White, M. J., Goodier, M. R., & Riley, E. M. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00422 · Cited by 282 · see citing works
Sittplangkoon, C., Alameh, M.-G., Weissman, D., Lin, P. J. C., Tam, Y. K., Prompetchara, E., & Palaga, T. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.983000 · Cited by 79 · see citing works
- Authors
- Lakshmi Narendra, B., Eshvendar Reddy, K., Shantikumar, S., & Ramakrishna, S.
- Affiliations
- National Institute of Pharmaceutical Education and Research (IN)
- Venue
- Inflammation Research
- Published
- 2013-07-19
- Volume
- 62
- Issue
- 9
- Pages
- 823-834
- ISSN
- 1023-3830 (ISSN-L)
- 1420-908X
- OpenAlex
- W2035105999
- Cited by
- 206
- References
- 93
- Citations by year
- 2026: 7 · 2025: 28 · 2024: 16 · 2023: 22 · 2022: 23 · 2021: 14 · 2020: 15 · 2019: 11 · 2018: 17 · 2017: 12 · 2016: 10 · 2015: 14 · 2014: 13 · 2013: 4
- FWCI
- 1.19
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Inflammation Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- tumor immune evasion, tumor surveillance, immunoediting, innate immunity, adaptive immunity, natural killer cells, tumor-associated macrophages, regulatory T cells, Th17 cells, myeloid-derived suppressor cells, CD8+ cytotoxic T lymphocytes, CD4+ T helper cells, interferon-gamma
- MeSH terms
- Humans, Immunity, Innate, Immunosuppression Therapy, Macrophages, Neoplasms, Cytokines, T-Lymphocytes, Regulatory, Adaptive Immunity, Th17 Cells
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