TGFβ and cancer metastasis: an inflammation link
Open accessAbstract
Dysregulated transforming growth factor beta (TGFbeta) signaling is observed in a variety of human cancers. TGFbeta is produced in large quantities by many tumor types and is known to be pro-oncogenic. Therapeutic strategies directed against TGFbeta signaling using neutralizing antibodies and small molecular inhibitors have been developed. However, TGFbeta is also found to function as a tumor suppressor. This switch from a tumor suppressor in premalignant stages of tumorigenesis to a tumor promoter in later stages of the disease poses great challenges in TGFbeta-targeted cancer therapy. It remains unclear what mechanisms underlie the dual role of TGFbeta and what factors mediate the switch. In the past, most work on dissecting underlying mechanisms was focused on differential regulation of signaling pathways by tumor cell autonomous TGFbeta signaling. Recent progress in elucidating TGFbeta effects on host immune/inflammatory reactions in the tumor microenvironment and distant organs brings exciting new perspectives to the field.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Cancer tissue is riddled with immune cells which support tumor growth, while inflammation is also evident at the whole-body level.
“Cancer tissue is riddled with immune cells which support tumor growth, while inflammation is also evident at the whole‐body level.33, 34”
From Hypoalbuminemia: Pathogenesis and Clinical Significance (2019) · cites this paper as [33]
The “Tumor microenvironment” section describes tumors as filled with inflammatory and immune cells and explains how some of these cells promote tumor progression. It also says other immune cells inhibit tumor development. The paper discusses immune and inflammatory responses in distant organs and systemic immune suppression, but does not establish the claim that inflammation is evident at the whole-body level. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Coussens, L. M., & Werb, Z. (2002) · Nature · doi:10.1038/nature01322 · Cited by 15,111 · see citing works
Mantovani, A., Allavena, P., Sica, A., & Balkwill, F. (2008) · Nature · doi:10.1038/nature07205 · Cited by 11,399 · see citing works
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
Type, Density, and Location of Immune Cells Within Human Colorectal Tumors Predict Clinical Outcome
Galon, J., Costes, A., Sanchez-Cabo, F., Kirilovsky, A., Mlecnik, B., Lagorce-Pagès, C., Tosolini, M., Camus, M., Berger, A., Wind, P., et al. (2006) · Science · doi:10.1126/science.1129139 · Cited by 6,516 · see citing works
Massagué, J. (2008) · Cell · doi:10.1016/j.cell.2008.07.001 · Cited by 3,907 · 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
Polarization of Tumor-Associated Neutrophil Phenotype by TGF-β: “N1” versus “N2” TAN
Fridlender, Z. G., Sun, J., Kim, S., Kapoor, V., Cheng, G., Ling, L. E., Worthen, G. S., & Albelda, S. Μ. (2009) · Cancer Cell · doi:10.1016/j.ccr.2009.06.017 · Cited by 3,382 · 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
Metastasis to bone: causes, consequences and therapeutic opportunities
Mundy, G. R. (2002) · Nature reviews. Cancer · doi:10.1038/nrc867 · Cited by 2,787 · see citing works
Macrophages: Obligate Partners for Tumor Cell Migration, Invasion, and Metastasis
Condeelis, J. S., & Pollard, J. W. (2006) · Cell · doi:10.1016/j.cell.2006.01.007 · Cited by 2,693 · see citing works
Paradoxical roles of the immune system during cancer development
de Visser, K. E., Eichten, A., & Coussens, L. M. (2006) · Nature reviews. Cancer · doi:10.1038/nrc1782 · Cited by 2,261 · see citing works
TRANSFORMING GROWTH FACTOR-β REGULATION OF IMMUNE RESPONSES
Li, M. O., Wan, Y. Y., Sanjabi, S., Robertson, A.-K. L., & Flavell, R. A. (2005) · Annual Review of Immunology · doi:10.1146/annurev.immunol.24.021605.090737 · Cited by 2,199 · see citing works
Stromal gene expression predicts clinical outcome in breast cancer
Finak, G., Bertos, N., Pepin, F., Sadekova, S., Souleimanova, M., Zhao, H., Chen, H., Ömeroğlu, G., Meterissian, S. H., Ömeroğlu, A., et al. (2008) · Nature Medicine · doi:10.1038/nm1764 · Cited by 1,687 · see citing works
Kruse, J.-P., & Gu, W. (2009) · Cell · doi:10.1016/j.cell.2009.04.050 · Cited by 1,610 · cited 1× · see citing works
“Do tumor suppressors other than TGFβ function as inflammatory suppressors? p53 is a very important tumor suppressor, regulating cell cycle, check point control, DNA damage/repair, and induction of apoptosis [ 67 ].”
TGF-ß Signaling in Fibroblasts Modulates the Oncogenic Potential of Adjacent Epithelia
Bhowmick, N. A., Chytil, A., Plieth, D., Gorska, A. E., Dumont, N., Shappell, S., Washington, M. K., Neilson, E. G., & Moses, H. L. (2004) · Science · doi:10.1126/science.1090922 · Cited by 1,401 · see citing works
TGF-β directly targets cytotoxic T cell functions during tumor evasion of immune surveillance
Thomas, D. A., & Massagué, J. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.10.012 · Cited by 1,355 · see citing works
DeNardo, D. G., Barreto, J., Andreu, P., Vásquez, L. J., Tawfik, D., Kolhatkar, N. S., & Coussens, L. M. (2009) · Cancer Cell · doi:10.1016/j.ccr.2009.06.018 · Cited by 1,340 · see citing works
Trophic macrophages in development and disease
Pollard, J. W. (2009) · Nature Reviews Immunology · doi:10.1038/nri2528 · Cited by 1,178 · see citing works
Hypoxia, DNA repair and genetic instability
Bristow, R. G., & Hill, R. P. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2344 · Cited by 1,140 · see citing works
Yang, L., DeBusk, L. M., Fukuda, K., Fingleton, B., Green-Jarvis, B., Shyr, Y., Matrisian, L. M., Carbone, D. P., & Lin, P. C. (2004) · Cancer Cell · doi:10.1016/j.ccr.2004.08.031 · Cited by 1,140 · see citing works
Self-citationDu, R., Lu, K. V., Petritsch, C. K., Liu, P., Ganß, R., Passegue, E. A., Song, H., VandenBerg, S. R., Johnson, R. S., Werb, Z., et al. (2008) · Cancer Cell · doi:10.1016/j.ccr.2008.01.034 · Cited by 1,131 · see citing works
Tenets of PTEN Tumor Suppression
Salmena, L., Carracedo, A., & Pandolfi, P. P. (2008) · Cell · doi:10.1016/j.cell.2008.04.013 · Cited by 1,033 · see citing works
Hiratsuka, S., Watanabe, A., Aburatani, H., & Maru, Y. (2006) · Nature Cell Biology · doi:10.1038/ncb1507 · Cited by 1,016 · see citing works
p53 and Human Cancer: The First Ten Thousand Mutations
Hainaut, P. L., & Hollstein, M. C. (1999) · Advances in cancer research · doi:10.1016/s0065-230x(08)60785-x · Cited by 980 · see citing works
TGFβ Primes Breast Tumors for Lung Metastasis Seeding through Angiopoietin-like 4
Padua, D. M., Zhang, X. H.-F., Wang, Q., Nadal, C., Gerald, W. L., Gomis, R. R., & Massagué, J. (2008) · Cell · doi:10.1016/j.cell.2008.01.046 · Cited by 947 · 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
TGF-β: A Master of All T Cell Trades
Li, M. O., & Flavell, R. A. (2008) · Cell · doi:10.1016/j.cell.2008.07.025 · Cited by 888 · see citing works
Molecular Predictors of Survival after Adjuvant Chemotherapy for Colon Cancer
Watanabe, T., Wu, T., Catalano, P. J., Ueki, T., Satriano, R., Haller, D. G., Benson, A. B., & Hamilton, S. R. (2001) · New England Journal of Medicine · doi:10.1056/nejm200104193441603 · Cited by 886 · see citing works
Role of tumor-associated macrophages in tumor progression and invasion
Mantovani, A., Schioppa, T., Porta, C., Allavena, P., & Sica, A. (2006) · Cancer and Metastasis Reviews · doi:10.1007/s10555-006-9001-7 · Cited by 885 · see citing works
Budhu, A., Forgues, M., Ye, Q.-H., Jia, H.-L., He, P., Zanetti, K. A., Kammula, U. S., Chen, Y., Qin, L., Tang, Z., et al. (2006) · Cancer Cell · doi:10.1016/j.ccr.2006.06.016 · Cited by 843 · see citing works
De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent
de Visser, K. E., Korets, L. V., & Coussens, L. M. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.04.014 · Cited by 826 · see citing works
A Mutant-p53/Smad Complex Opposes p63 to Empower TGFβ-Induced Metastasis
Adorno, M., Cordenonsi, M., Montagner, M., Dupont, S., Wong, C., Hann, B. C., Solari, A., Bobisse, S., Rondina, M. B., Guzzardo, V., et al. (2009) · Cell · doi:10.1016/j.cell.2009.01.039 · Cited by 783 · see citing works
Modulation of the antitumor immune response by complement
Markiewski, M. M., DeAngelis, R. A., Benencia, F., Ricklin-Lichtsteiner, S. K., Koutoulaki, A., Gerard, C. J., Coukos, G., & Lambris, J. D. (2008) · Nature Immunology · doi:10.1038/ni.1655 · Cited by 770 · see citing works
Serafini, P., Borrello, I., & Bronte, V. (2005) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2005.07.005 · Cited by 758 · see citing works
NKT cell–mediated repression of tumor immunosurveillance by IL-13 and the IL-4R–STAT6 pathway
Terabe, M., Matsui, S., Noben-Trauth, N., Chen, H., Watson, L. C., Donaldson, D. D., Carbone, D. P., Paul, W. E., & Berzofsky, J. A. (2000) · Nature Immunology · doi:10.1038/82771 · Cited by 698 · see citing works
Mantovani, A. (2008) · Nature · doi:10.1038/457036b · Cited by 646 · see citing works
Balkwill, F. R., & Coussens, L. M. (2004) · Nature · doi:10.1038/431405a · Cited by 627 · see citing works
Intestinal Tumorigenesis in Compound Mutant Mice of both Dpc4(Smad4) and Apc Genes
Takaku, K., Oshima, M., Miyoshi, H., Matsui, M., Seldin, M. F., & Taketo, M. M. (1998) · Cell · doi:10.1016/s0092-8674(00)81132-0 · Cited by 610 · see citing works
Tumor‐induced tolerance and immune suppression by myeloid derived suppressor cells
Marigo, I., Dolcetti, L., Serafini, P., Zanovello, P., & Bronte, V. (2008) · Immunological Reviews · doi:10.1111/j.1600-065x.2008.00602.x · Cited by 608 · see citing works
FcRγ Activation Regulates Inflammation-Associated Squamous Carcinogenesis
Andreu, P., Johansson, M., Affara, N. I., Pucci, F., Tan, T., Junankar, S. R., Korets, L. V., Lam, J., Tawfik, D., DeNardo, D. G., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2009.12.019 · Cited by 592 · see citing works
Terabe, M., Matsui, S., Park, J.-M., Mamura, M., Noben-Trauth, N., Donaldson, D. D., Chen, W., Wahl, S. M., Ledbetter, S. R., Pratt, B. M., et al. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20022227 · Cited by 533 · see citing works
Pten in stromal fibroblasts suppresses mammary epithelial tumours
Trimboli, A. J., Cantemir-Stone, C. Z., Li, F., Wallace, J. A., Merchant, A. S., Creasap, N., Thompson, J. C., Caserta, E., Wang, H., Chong, J.-L., et al. (2009) · Nature · doi:10.1038/nature08486 · Cited by 501 · see citing works
FAM/USP9x, a Deubiquitinating Enzyme Essential for TGFβ Signaling, Controls Smad4 Monoubiquitination
Dupont, S., Mamidi, A., Cordenonsi, M., Montagner, M., Zacchigna, L., Adorno, M., Martello, G., Stinchfield, M. J., Soligo, S., Morsut, L., et al. (2009) · Cell · doi:10.1016/j.cell.2008.10.051 · Cited by 494 · see citing works
Hussain, S. P., Amstad, P., Raja, K., Ambs, S., Nagashima, M., Bennett, W. P., Shields, P. G., Ham, A. L., Swenberg, J. A., Marrogi, A. J., et al. (2000) · PubMed · Cited by 482 · see citing works
Bruna, A., Darken, R. S., Rojo, F., Ocaña, A., Peñuelas, S., Arias, A., Parı́s, R., Tortosa, A., Mora, J., Baselga, J. M., et al. (2007) · Cancer Cell · doi:10.1016/j.ccr.2006.11.023 · Cited by 472 · see citing works
Nuclear cytokine-activated IKKα controls prostate cancer metastasis by repressing Maspin
Luo, J., Tan, W., Ricono, J. M., Korchynskyi, O., Zhang, M., Gonias, S. L., Cheresh, D. A., & Karin, M. (2007) · Nature · doi:10.1038/nature05656 · Cited by 436 · see citing works
Peng, G., Wang, H. Y., Peng, W., Kiniwa, Y., Seo, K. H., & Wang, R. (2007) · Immunity · doi:10.1016/j.immuni.2007.05.020 · Cited by 408 · see citing works
Ijichi, H., Chytil, A., Gorska, A. E., Aakre, M. E., Fujitani, Y., Fujitani, S., Wright, C. V. E., & Moses, H. L. (2006) · Genes & Development · doi:10.1101/gad.1475506 · Cited by 379 · see citing works
Biswas, S., Guix, M., Rinehart, C., Dugger, T. C., Chytil, A. M., Moses, H. L., Freeman, M. L., & Arteaga, C. L. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30740 · Cited by 346 · see citing works
Inhibitory Effects of B Cells on Antitumor Immunity
Inoue, S., Leitner, W. W., Golding, B., & Scott, D. E. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3766 · Cited by 338 · see citing works
Smad4 signalling in T cells is required for suppression of gastrointestinal cancer
Kim, B., Li, C., Qiao, W., Mamura, M., Kasperczak, B., Anver, M. R., Wolfraim, L. A., Hong, S., Mushinski, E. B., Potter, M., et al. (2006) · Nature · doi:10.1038/nature04846 · Cited by 320 · see citing works
SMAD4-deficient intestinal tumors recruit CCR1+ myeloid cells that promote invasion
Kitamura, T., Kometani, K., Hashida, H., Matsunaga, A., Miyoshi, H., Hosogi, H., Aoki, M., Oshima, M., Hattori, M., Takabayashi, A., et al. (2007) · Nature Genetics · doi:10.1038/ng1997 · Cited by 282 · see citing works
The ‘short’ history of regulatory B cells
Mauri, C., & Ehrenstein, M. R. (2007) · Trends in Immunology · doi:10.1016/j.it.2007.10.004 · Cited by 281 · see citing works
Guasch, G., Schöber, M., Pasolli, H. A., Conn, E. B., Polak, L., & Fuchs, E. V. (2007) · Cancer Cell · doi:10.1016/j.ccr.2007.08.020 · Cited by 267 · see citing works
Nam, J., Terabe, M., Kang, M., Chae, H., Voong, N., Yang, Y.-A., Laurence, A. D. J., Michalowska, A. M., Mamura, M., Lonning, S. M., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0206 · Cited by 250 · see citing works
Forrester, E., Chytil, A., Bierie, B., Aakre, M. E., Gorska, A. E., Sharif‐Afshar, A., Muller, W. J., & Moses, H. L. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-3272 · Cited by 248 · see citing works
Nam, J., Terabe, M., Mamura, M., Kang, M., Chae, H., Stuelten, C. H., Kohn, E. A., Tang, B., Sabzevari, H., Anver, M. R., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0215 · Cited by 233 · see citing works
TGF‐β: a mobile purveyor of immune privilege
Wahl, S. M., Wen, J., & Moutsopoulos, N. M. (2006) · Immunological Reviews · doi:10.1111/j.1600-065x.2006.00437.x · Cited by 228 · see citing works
Helicobacter Infection Is Required for Inflammation and Colon Cancer in Smad3-Deficient Mice
Maggio‐Price, L., Treuting, P. M., Zeng, W., Tsang, M., Bielefeldt‐Ohmann, H., & Iritani, B. M. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-2448 · Cited by 209 · see citing works
Lu, S., Herrington, H. C., Reh, D. D., Weber, S. M., Bornstein, S., Wang, D., Li, A. G., Tang, C.-F., Siddiqui, Y., Nord, J., et al. (2006) · Genes & Development · doi:10.1101/gad.1413306 · Cited by 204 · see citing works
Elimination of colon cancer in germ-free transforming growth factor beta 1-deficient mice.
Engle, S. J., Ormsby, I., Pawlowski, S. A., Boivin, G. P., Croft, J., Balish, E., & Doetschman, T. C. (2002) · PubMed · Cited by 199 · see citing works
Lu, S., Reh, D. D., Li, A. G., Woods, J., Corless, C. L., Kulesz-Martin, M. F., & Wang, X. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-1032 · Cited by 197 · see citing works
Demotte, N., Stroobant, V., Courtoy, P. J., Smissen, P. V. D., Colau, D., Luescher, I. F., Hivroz, C., Nicaise, J., Squifflet, J.-L., Mourad, M., et al. (2008) · Immunity · doi:10.1016/j.immuni.2008.01.011 · Cited by 181 · see citing works
Immune Enhancement of Skin Carcinogenesis by CD4+ T Cells
Daniel, D., Meyer-Morse, N., Bergsland, E. K., Dehne, K., Coussens, L. M., & Hanahan, D. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20021047 · Cited by 180 · see citing works
Liu, I. M., Schilling, S. H., Knouse, K. A., Choy, L., Derynck, R., & Wang, X. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.266 · Cited by 174 · see citing works
Muñoz, N. M., Upton, M. P., Muñoz-Rojas, A. R., Washington, M. K., Li, L., Chytil, A. M., Sözmen, E. G., Madison, B., Pozzi, A., Moon, R. T., et al. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-0890 · Cited by 168 · see citing works
Fas ligand–mediated paracrine T cell regulation by the receptor NKG2D in tumor immunity
Groh, V., Smythe, K. S., Dai, Z., & Spies, T. A. (2006) · Nature Immunology · doi:10.1038/ni1350 · Cited by 167 · see citing works
Biswas, S., Chytil, A. M., Washington, K., Romero–Gallo, J., Gorska, A. E., Wirth, P. S., Gautam, S., Moses, H. L., & Grady, W. M. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-3255 · Cited by 153 · 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
The Yin-Yang of Tumor-Associated Neutrophils
Mantovani, A. (2009) · Cancer Cell · doi:10.1016/j.ccr.2009.08.014 · Cited by 148 · see citing works
Monteleone, G., Mann, J., Monteleone, I., Vavassori, P., Bremner, R., Fantini, M. C., Blanco, G. D. V., Tersigni, R., Alessandroni, L., Mann, D. A., et al. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m303654200 · Cited by 148 · see citing works
NKT cells in immunoregulation of tumor immunity: a new immunoregulatory axis
Terabe, M., & Berzofsky, J. A. (2007) · Trends in Immunology · doi:10.1016/j.it.2007.05.008 · Cited by 145 · see citing works
Bierie, B., Stover, D. G., Abel, T. W., Chytil, A. M., Gorska, A. E., Aakre, M. E., Forrester, E., Yang, H. H., Wagner, K., & Moses, H. L. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-5597 · Cited by 124 · see citing works
Lu, T., Tian, L., Han, Y., Vogelbaum, M., & Stark, G. R. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700118104 · Cited by 113 · see citing works
Nitric Oxide Is a Key Component in Inflammation-Accelerated Tumorigenesis
Hussain, S. P., He, P., Subleski, J. J., Hofseth, L. J., Trivers, G. E., Mechanic, L. E., Hofseth, A. B., Bernard, M., Schwank, J., Nguyen, G. H., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0410 · Cited by 108 · see citing works
Inhibition of TGFβ signaling in cancer therapy
Arteaga, C. L. (2005) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2005.12.009 · Cited by 105 · see citing works
Rolny, C., Capparuccia, L., Casazza, A., Mazzone, M., Vallario, A., Cignetti, A., Médico, E., Carmeliet, P., Comoglio, P. M., & Tamagnone, L. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20072509 · Cited by 105 · see citing works
Ruzankina, Y., Schoppy, D. W., Asare, A., Clark, C. E., Vonderheide, R. H., & Brown, E. J. (2009) · Nature Genetics · doi:10.1038/ng.441 · Cited by 104 · see citing works
Farazi, P. A., Zeisberg, M., Glickman, J. N., Zhang, Y., Kalluri, R., & DePinho, R. A. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-4609 · Cited by 99 · see citing works
Cancer's Bulwark Against Immune Attack: MDS Cells
Marx, J. L. (2008) · Science · doi:10.1126/science.319.5860.154 · Cited by 77 · see citing works
The dual adverse effects of TGF-β secretion on tumor progression
Trapani, J. A. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.10.018 · Cited by 77 · see citing works
Lee, T., Yang, X. P., Yan, B., Friedman, J., Duggal, P., Bagain, L., Dong, G., Yeh, N. T., Wang, J., Zhou, J., et al. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-0670 · Cited by 76 · see citing works
Gain or loss of TGF-β signaling in mammary carcinoma cells can promote metastasis
Bierie, B., & Moses, H. L. (2009) · Cell Cycle · doi:10.4161/cc.8.20.9727 · Cited by 60 · see citing works
Hong, S., Lee, C., & Kim, S. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-1179 · Cited by 52 · see citing works
Metastasis Suppressors and the Tumor Microenvironment
Bodenstine, T. M., & Welch, D. R. (2008) · Cancer Microenvironment · doi:10.1007/s12307-008-0001-8 · Cited by 39 · see citing works
Fujita, T., Teramoto, K., Ozaki, Y., Hanaoka, J., Tezuka, N., Itoh, Y., Asai, T., Fujino, S., Kontani, K., & Ogasawara, K. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-2499 · Cited by 35 · see citing works
Taylor, J. L., Hickson, J. A., Lotan, T. L., Yamada, D., & Rinker-Schaeffer, C. W. (2007) · Cancer and Metastasis Reviews · doi:10.1007/s10555-007-9106-7 · Cited by 30 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Hypoalbuminemia: Pathogenesis and Clinical Significance
Soeters, P. B., Wolfe, R. R., & Shenkin, A. (2019) · Journal of Parenteral and Enteral Nutrition · doi:10.1002/jpen.1451 · Cited by 1,448 · see citing works
Targeting the TGFβ pathway for cancer therapy
Neuzillet, C., Tijeras‐Raballand, A., Cohen, R., Cros, J. F., Faivre, S. J., Raymond, É., & Gramont, A. D. E. (2014) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.11.001 · Cited by 610 · see citing works
Tissue invasion and metastasis: Molecular, biological and clinical perspectives
Jiang, W. G., Sanders, A. J., Katoh, M., Ungefroren, H., Gieseler, F., Prince, M. E., Thompson, S. K., Zollo, M., Spano, D., Dhawan, P., et al. (2015) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2015.03.008 · Cited by 514 · see citing works
TGF-β signalling and its role in cancer progression and metastasis
Drabsch, Y., & ten Dijke, P. (2012) · Cancer and Metastasis Reviews · doi:10.1007/s10555-012-9375-7 · Cited by 430 · see citing works
Cancer immunology—analysis of host and tumor factors for personalized medicine
Ogino, S., Galon, J., Fuchs, C. S., & Dranoff, G. (2011) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2011.122 · Cited by 284 · see citing works
Therapeutic Cancer Vaccines: Current Status and Moving Forward
Schlom, J. (2012) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djs033 · Cited by 279 · see citing works
Guo, L., Chen, C., Shi, M., Wang, F., Chen, X., Diao, D., Hu, M., Yu, M., Lu, Q., & Guo, N. (2013) · Oncogene · doi:10.1038/onc.2012.573 · Cited by 209 · see citing works
Transforming Growth Factor-β in the Gastrointestinal and Hepatic Tumor Microenvironment
Achyut, B. R., & Yang, H. H. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.07.048 · Cited by 200 · see citing works
The neuronal influence on tumor progression
Mancino, M., Ametller, E., Gascón, P., & Almendro, V. (2011) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2011.04.005 · Cited by 158 · see citing works
Yang, H. H., & Lin, P. C. (2017) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2017.08.001 · Cited by 156 · see citing works
Duan, W., Yang, L., Liu, J., Dai, Z., Wang, Z., Zhang, H., Zhang, X., Liang, X., Luo, P., Zhang, J., et al. (2023) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.14489 · Cited by 153 · see citing works
Self-citationPerspectives of TGF-β inhibition in pancreatic and hepatocellular carcinomas
Neuzillet, C., Gramont, A. D. E., Tijeras‐Raballand, A., de Mestier, L., Cros, J. F., Faivre, S. J., & Raymond, É. (2013) · Oncotarget · doi:10.18632/oncotarget.1569 · Cited by 144 · see citing works
Association of oral dysbiosis with oral cancer development (Review)
Rosa, G. R. M. L., Gattuso, G., Pedull�, E., Rapisarda, E., Nicolosi, D., & Salmeri, M. (2020) · Oncology Letters · doi:10.3892/ol.2020.11441 · Cited by 125 · see citing works
Cancer metastasis as a non-healing wound
Deyell, M., Garris, C., & Laughney, A. M. (2021) · British Journal of Cancer · doi:10.1038/s41416-021-01309-w · Cited by 112 · see citing works
Dichotomous roles of TGF-β in human cancer
Huang, J. J., & Blobe, G. C. (2016) · Biochemical Society Transactions · doi:10.1042/bst20160065 · Cited by 108 · see citing works
Expansion and functions of myeloid-derived suppressor cells in the tumor microenvironment
Qu, P., Wang, L., & Lin, P. C. (2015) · Cancer Letters · doi:10.1016/j.canlet.2015.10.022 · Cited by 103 · see citing works
Achyut, B. R., Bader, D. A., Robles, A. I., Wangsa, D., Harris, C. C., Ried, T., & Yang, H. H. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003251 · Cited by 77 · see citing works
Pang, X., Tang, Y., & Liang, X. (2018) · Oncology Letters · doi:10.3892/ol.2018.9319 · Cited by 69 · see citing works
The role played by the microenvironment in site-specific metastasis
Klein-Goldberg, A., Maman, S., & Witz, I. P. (2013) · Cancer Letters · doi:10.1016/j.canlet.2013.08.029 · Cited by 64 · see citing works
Yu, L., Di, Y., Xin, L., Ren, Y., Liu, X., Sun, X., Zhang, W., Yao, Z., & Yang, J. (2017) · Oncogene · doi:10.1038/onc.2017.30 · Cited by 62 · see citing works
Roles of tumor suppressors in regulating tumor-associated inflammation
Yang, L., & Karin, M. (2014) · Cell Death and Differentiation · doi:10.1038/cdd.2014.131 · Cited by 58 · see citing works
Self-citationTGF-β and Restenosis Revisited: A Smad Link
Suwanabol, P. A., Kent, K. C., & Liu, B. (2011) · Journal of Surgical Research · doi:10.1016/j.jss.2010.12.020 · Cited by 55 · see citing works
The Role of TGF-β during Pregnancy and Pregnancy Complications
Wen, B., Liao, H., Lin, W., Li, Z., Ma, X.-Q., Xu, Q., & Yu, F. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242316882 · Cited by 54 · see citing works
Yang, Y., Xu, W., Peng, D., Wang, H., Zhang, X., Wang, H., Xiao, F., Zhu, Y., Ji, Y., Gulukota, K., et al. (2019) · Human Gene Therapy · doi:10.1089/hum.2019.059 · Cited by 50 · see citing works
Autoimmunity as a Double Agent in Tumor Killing and Cancer Promotion
Toomer, K. H., & Chen, Z. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00116 · Cited by 44 · see citing works
Löffek, S. (2018) · Journal of Oncology · doi:10.1155/2018/9732939 · Cited by 44 · see citing works
The inflammasome: an emerging therapeutic oncotarget for cancer prevention
Zhiyu, W., Wang, N., Wang, Q., Peng, C. Y., Zhang, J., Liu, P., Ou, A., Zhong, S., Cordero, M. D., & Lin, Y. (2016) · Oncotarget · doi:10.18632/oncotarget.9391 · Cited by 43 · see citing works
Zhao, J., Liu, J., Lee, J.-F., Zhang, W., Kandouz, M., VanHecke, G. C., Chen, S., Ahn, Y., Lonardo, F., & Lee, M.-J. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.740084 · Cited by 43 · see citing works
Mesenchymal ovarian cancer cells promote CD8+ T cell exhaustion through the LGALS3-LAG3 axis
Yakubovich, E., Cook, D. P., Rodriguez, G. M., & Vanderhyden, B. C. (2023) · npj Systems Biology and Applications · doi:10.1038/s41540-023-00322-4 · Cited by 38 · see citing works
Microbiota, Epithelium, Inflammation, and TGF-β Signaling: An Intricate Interaction in Oncogenesis
Pang, X., Tang, Y.-J., Ren, X., Chen, Q., Tang, Y., & Liang, X. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01353 · Cited by 37 · see citing works
EMT and Inflammation: Crossroads in HCC
Şengez, B., Carr, B. I., & Alotaibi, H. (2022) · Journal of Gastrointestinal Cancer · doi:10.1007/s12029-021-00801-z · Cited by 37 · see citing works
Abdullah, N. A., Hashim, N. F. M., Ammar, A., & Zakuan, N. M. (2021) · Molecules · doi:10.3390/molecules26040775 · Cited by 34 · see citing works
TGF-β1 mediates the radiation response of prostate cancer
Wu, C., Hsieh, C., Yen, T., Chen, W., & Chen, M. (2014) · Journal of Molecular Medicine · doi:10.1007/s00109-014-1206-6 · Cited by 34 · see citing works
Elahi, M., Rakhshan, V., Taghavi, N., & Moshref, M. (2011) · Biomarkers · doi:10.3109/1354750x.2011.635804 · Cited by 33 · see citing works
Wang, H., Wang, P., Xu, M. M., Song, X., Wu, H. M., Evert, M., Calvisi, D. F., Zeng, Y., & Chen, X. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-03488-z · Cited by 32 · see citing works
Seher, A., Nickel, J., Mueller, T. D., Kneitz, S., Gebhardt, S., Meyer‐ter‐Vehn, T., Schlunck, G., & Sebald, W. (2011) · Europe PMC (PubMed Central) · Cited by 32 · see citing works
Microbial deprivation, inflammation and cancer
von Hertzen, L. C., Joensuu, H., & Haahtela, T. (2011) · Cancer and Metastasis Reviews · doi:10.1007/s10555-011-9284-1 · Cited by 31 · see citing works
Abdelkarim, M., Vintonenko, N., Starzec, A. B., Robles, A., Aubert, J., Martin‐Magniette, M., Mourah, S., Podgorniak, M.-P., Rodrigues-Ferreira, S., Nahmias, C., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023334 · Cited by 27 · see citing works
The conditional role of inflammation in pregnancy and cancer
Soeters, P. B., & Grimble, R. F. (2013) · Clinical Nutrition · doi:10.1016/j.clnu.2012.07.010 · Cited by 24 · see citing works
Macrophage coculture enhanced invasion of gastric cancer cells via TGF-β and BMP pathways
Shen, Z., Kauttu, T., Cao, J., Seppänen, H. E., Vainionpää, S., Ye, Y., Wang, S., Mustonen, H. K., & Puolakkainen, P. A. (2013) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365521.2013.772226 · Cited by 23 · see citing works
Pregnancy and Cancer: Cellular Biology and Mechanisms Affecting the Placenta
Oliveira, M. D. M. S., Salgado, C. D. M., Viana, L. R., & Gomes‐Marcondes, M. C. C. (2021) · Cancers · doi:10.3390/cancers13071667 · Cited by 18 · see citing works
Bonowicz, K., Mikołajczyk, K., Faisal, I., Qamar, M., Steinbrink, K., Kleszczyński, K., Grzanka, A., & Gagat, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232315335 · Cited by 18 · see citing works
Wang, J., Cheng, F. H. C., Tedrow, J., Chang, W., Zhang, C., & Mitra, A. K. (2020) · Cancers · doi:10.3390/cancers12113184 · Cited by 17 · see citing works
Modulation of YY1 and p53 expression by transforming growth factor-β3 in prostate cell lines
Caggia, S., Libra, M., Malaponte, G., & Cardile, V. (2011) · Cytokine · doi:10.1016/j.cyto.2011.06.024 · Cited by 13 · see citing works
T cell- but not tumor cell-produced TGF-β1 promotes the development of spontaneous mammary cancer
Sarkar, A., Donkor, M. K., & Li, M. O. (2011) · Oncotarget · doi:10.18632/oncotarget.403 · Cited by 14 · see citing works
Elahi, M., & Rakhshan, V. (2020) · Scientific Reports · doi:10.1038/s41598-020-65145-3 · Cited by 12 · see citing works
Wang, Z., Wang, N., Zheng, Y., & Wang, S. (2018) · Experientia supplementum · doi:10.1007/978-3-319-89390-7_12 · Cited by 9 · see citing works
Clinicopathologic Characterization of Prostatic Cancer in Dogs
Vasilatis, D. M., & Ghosh, P. (2024) · Animals · doi:10.3390/ani14040588 · Cited by 7 · see citing works
Dias, V., Alves, Â., Medeiros, R., Teixeira, A. L., & Dias, F. (2025) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2025.189372 · Cited by 5 · see citing works
Rowaiye, A. B., Njoku, M. O., Oli, A. N., Akrami, S., Asala, T., Uzochukwu, I. C., Akpa, A., Saki, M., & Esimone, C. O. (2021) · ONCOLOGIE · doi:10.32604/oncologie.2021.019738 · Cited by 6 · see citing works
Li, Z., Zhang, Y. N., Li, D., Du, X., Chen, L., & Guo, Y. (2024) · Neuroscience · doi:10.1016/j.neuroscience.2024.11.053 · Cited by 4 · see citing works
Wang, P., Zhuang, W., Zheng, Z., Zhang, L., Zhang, X., & Chen, Q. (2023) · Clinical & Experimental Immunology · doi:10.1093/cei/uxad073 · Cited by 4 · see citing works
Brain metastasis in non‐small cell lung cancer: High‐risk factors and predictive models
Chen, G., Zhao, B., Mao, S., Liu, Q., Zhao, Y., Liu, Y., Luo, Y., & Li, Q. (2025) · Open Research (University of Surrey) · doi:10.1002/viw.20250046 · Cited by 3 · see citing works
The underlying metabolism of hypoalbuminemia and its clinical effects
Soeters, P. B., & de Leeuw, P. W. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-820205-0.00010-4 · Cited by 3 · see citing works
Gao, D., & Li, S. (2013) · Pathology & Oncology Research · doi:10.1007/s12253-013-9734-x · Cited by 3 · see citing works
Cyclopamine targeting hedgehog modulates nuclear control of the osteoblast activity
Fernandes, C. J. D. C., Ferreira, M. R., & Zambuzzi, W. F. (2023) · Cells and Development · doi:10.1016/j.cdev.2023.203836 · Cited by 2 · see citing works
Mechanism Analyses for Elucidating the Role of LOXL2 Silencing in Hepatocellular Carcinoma
Wu, L., Zhang, Y., Zhu, Y., Cong, Q., Xiang, Y., & Fu, L. (2015) · Journal of Agricultural Science and Technology A · doi:10.17265/2161-6256/2015.05.009 · Cited by 1 · see citing works
Elahi, M., & Rakhshan, V. (2022) · Advances in Preventive Medicine · doi:10.1155/2022/3145117 · Cited by 1 · see citing works
Dhawan, U., Wang, W.-L., Lin, Y., Yang, R., Dalby, M. J., Salmerón‐Sánchez, M., & Yu, H. (2023) · Nano Today · doi:10.1016/j.nantod.2023.101882 · Cited by 1 · see citing works
Aberrant expression of CD14 in breast tumor cells is associated with poor outcomePreprint
Katayama, H., Dou, R., Léon-Letelier, R. A., Irajizad, E., Sevillano, A. M., Park, S., Hsiao, F. C., Cai, Y., Vykoukal, J., Fahrmann, J. F., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.07.622456 · Cited by 1 · see citing works
Comparable metabolism in pregnancy and cancer: A universal role of the Warburg effect
Soeters, P. B., & de Leeuw, P. W. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-820205-0.00018-9
Fernandes, C., & Zambuzzi, W. F. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4052319
Caractérisation moléculaire et immunité des cancers du sein triple-négatifs
Bonsang‐Kitzis, H. (2018) · theses.fr (ABES) · doi:10.70675/285c912cz8251z4099z9cf7ze121cd7350d0
Salem, S., Hamdy, R., Shakartalla, S. B., Halawy, D., Hashim, S., Remmani, N. B., Almehdi, A. M., & Soliman, S. S. M. (2026) · RSC Medicinal Chemistry · doi:10.1039/d6md00400h
- Authors
- Yang, L.
- Venue
- Cancer and Metastasis Reviews
- Published
- 2010-05-02
- Volume
- 29
- Issue
- 2
- Pages
- 263-271
- ISSN
- 0167-7659 (ISSN-L)
- 1573-7233
- PMC
- PMC6640647
- OpenAlex
- W2049952383
- Cited by
- 65
- References
- 87
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 3 · 2023: 6 · 2022: 4 · 2021: 7 · 2020: 3 · 2019: 1 · 2018: 6 · 2017: 2 · 2016: 3 · 2015: 3 · 2014: 5 · 2013: 6 · 2012: 3
- FWCI
- 0.53
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Cancer and Metastasis Reviews (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (Z99 CA999999)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mechanisms of cancer metastasis
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- TGF-beta signaling, metastasis, inflammation, tumor microenvironment, tumor suppressor, tumor promoters, host immune response
- MeSH terms
- Humans, Inflammation, Neoplasm Metastasis, Neoplasms, Signal Transduction, Genes, Tumor Suppressor, Transforming Growth Factor beta
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