Quantitation of TGF-β proteins in mouse tissues shows reciprocal changes in TGF-β1 and TGF-β3 in normal vs neoplastic mammary epithelium
Open accessAbstract
// Kathleen C. Flanders 1, * , Yu-an Yang 1, * , Michelle Herrmann 1 , JinQiu Chen 1 , Nerissa Mendoza 2 , Amer M. Mirza 2 , Lalage M. Wakefield 1 1 Laboratory of Cancer Biology and Genetics, National Cancer Institute, Bethesda, Maryland, United States of America 2 XOMA Corporation, Berkeley, California, United States of America * These authors have contributed equally to this work Correspondence to: Kathleen C. Flanders, e-mail: flanderk@mail.nih.gov Keywords: TGF-β isoforms, protein, quantitation, mouse tissues, mammary gland Received: October 28, 2015 Accepted: April 26, 2016 Published: May 17, 2016 ABSTRACT Transforming growth factor-βs (TGF-βs) regulate tissue homeostasis, and their expression is perturbed in many diseases. The three isoforms (TGF-β1, -β2, and -β3) have similar bioactivities in vitro but show distinct activities in vivo. Little quantitative information exists for expression of TGF-β isoform proteins in physiology or disease. We developed an optimized method to quantitate protein levels of the three isoforms, using a Luminex® xMAP®-based multianalyte assay following acid-ethanol extraction of tissues. Analysis of multiple tissues and plasma from four strains of adult mice showed that TGF-β1 is the predominant isoform with TGF-β2 being ~10-fold lower. There were no sex-specific differences in isoform expression, but some tissues showed inter-strain variation, particularly for TGF-β2. The only adult tissue expressing appreciable TGF-β3 was the mammary gland, where its levels were comparable to TGF-β1. In situ hybridization showed the luminal epithelium as the major source of all TGF-β isoforms in the normal mammary gland. TGF-β1 protein was 3-8-fold higher in three murine mammary tumor models than in normal mammary gland, while TGF-β3 protein was 2-3-fold lower in tumors than normal tissue, suggesting reciprocal regulation of these isoforms in mammary tumorigenesis.
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?
TGF-β may contribute to the expansion of the fibroblast population.
“and in this way may contribute to the expansion of the fibroblast population250”
From TGFβ biology in cancer progression and immunotherapy (2021) · cites this paper as [250]
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
Gene expression profiling predicts clinical outcome of breast cancer
van 't Veer, L. J., Dai, H., van de Vijver, M. J., He, Y. D., Hart, A. A. M., Mao, M., Peterse, H. L., van der Kooy, K., Marton, M. J., Witteveen, A. T., et al. (2002) · Nature · doi:10.1038/415530a · Cited by 9,536 · 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 · cited 1× · see citing works
“Since tumors have been described as “wounds that do not heal” [55], and TGF-β3 opposes the actions of TGF-β1 in normal wound healing [13], the high expression of TGF-β3 in breast cancer progression may be protective through suppression of aberrantly engaged or persistent wound healing responses.”
Massagué, J. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3434 · Cited by 3,130 · see citing works
Assoian, R. K., Komoriya, A., Meyers, C. A., Miller, D. M., & Sporn, M. B. (1983) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)32345-7 · Cited by 1,597 · see citing works
Targeting the TGFβ signalling pathway in disease
Akhurst, R. J., & Hata, A. (2012) · Nature Reviews Drug Discovery · doi:10.1038/nrd3810 · Cited by 1,466 · see citing works
Sanford, L. P., Ormsby, I., Groot, A. C. G.-D., Sariola, H., Friedman, R., Boivin, G. P., Cardell, E. L., & Doetschman, T. (1997) · Development · doi:10.1242/dev.124.13.2659 · Cited by 1,447 · see citing works
Aslakson, C. J., & Miller, F. R. (1992) · PubMed · Cited by 1,234 · see citing works
Shah, M., Foreman, D. M., & Ferguson, M. W. J. (1995) · Journal of Cell Science · doi:10.1242/jcs.108.3.985 · Cited by 1,168 · see citing works
Chang, H. Y., Nuyten, D. S. A., Sneddon, J. B., Hastie, T., Tibshirani, R., Sørlie, T., Dai, H., He, Y. D., van't Veer, L. J., Bartelink, H., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409462102 · Cited by 981 · see citing works
Chang, H. Y., Sneddon, J. B., Alizadeh, A. A., Sood, R., West, R. B., Montgomery, K. D., Chi, J., van de Rijn, M., Botstein, D., & Brown, P. O. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020007 · Cited by 952 · see citing works
Transforming growth factor–β3 is required for secondary palate fusion
Proetzel, G., Pawlowski, S. A., Wiles, M. V., Yin, M., Boivin, G. P., Howles, P. N., Ding, J., Ferguson, M. W. J., & Doetschman, T. (1995) · Nature Genetics · doi:10.1038/ng1295-409 · Cited by 908 · see citing works
Betaglycan presents ligand to the TGFβ signaling receptor
López‐Casillas, F., Wrana, J. L., & Massagué, J. (1993) · Cell · doi:10.1016/0092-8674(93)90368-z · Cited by 892 · 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
Cancer Exosomes Trigger Fibroblast to Myofibroblast Differentiation
Webber, J. P., Steadman, R., Mason, M. D., Tabi, Z., & Clayton, A. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-1722 · Cited by 850 · see citing works
TGF-β signaling: positive and negative effects on tumorigenesis
Wakefield, L. M. (2002) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(01)00259-3 · Cited by 827 · see citing works
Self-citationAbe, M., Harpel, J. G., Metz, C. N., Nunes, I., Loskutoff, D. J., & Rifkin, D. B. (1994) · Analytical Biochemistry · doi:10.1006/abio.1994.1042 · Cited by 757 · see citing works
TGF- β signaling in cancer – a double-edged sword
Akhurst, R. J., & Derynck, R. (2001) · Trends in Cell Biology · doi:10.1016/s0962-8924(01)02130-4 · Cited by 756 · see citing works
Pelton, R. W., Saxena, B., Jones, M., Moses, H. L., & Gold, L. I. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.115.4.1091 · Cited by 671 · see citing works
Role of transforming growth factor-β superfamily signaling pathways in human disease
Gordon, K. J., & Blobe, G. C. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2008.01.006 · Cited by 644 · see citing works
Whole Animal Perfusion Fixation for Rodents
Gage, G. J., Kipke, D. R., & Shain, W. G. (2012) · Journal of Visualized Experiments · doi:10.3791/3564 · Cited by 523 · see citing works
Millan, F. A., Denhez, F., Kondaiah, P., & Akhurst, R. J. (1991) · Development · doi:10.1242/dev.111.1.131 · Cited by 498 · see citing works
Roberts, A. B., Lamb, L. C., Newton, D., Sporn, M. B., Larco, J. E. D., & Todaro, G. J. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.6.3494 · Cited by 448 · see citing works
Danielpour, D., Dart, L. L., Flanders, K. C., Roberts, A. B., & Sporn, M. B. (1989) · Journal of Cellular Physiology · doi:10.1002/jcp.1041380112 · Cited by 441 · see citing works
Self-citationTransgenic mice with increased plasma levels of TGF-beta 1 develop progressive renal disease.
Kopp, J. B., Factor, V. M., Mozes, M., Nagy, P., Sanderson, N., Böttinger, E. P., Klotman, P. E., & Thorgeirsson, S. S. (1996) · PubMed · Cited by 422 · see citing works
Mammary development in the embryo and adult: a journey of morphogenesis and commitment
Watson, C. J., & Khaled, W. T. (2008) · Development · doi:10.1242/dev.005439 · Cited by 414 · see citing works
Immunohistochemical localization of growth factors in fetal wound healing
Whitby, D. J., & Ferguson, M. W. J. (1991) · Developmental Biology · doi:10.1016/s0012-1606(05)80018-1 · Cited by 409 · see citing works
Frolik, C. A., Dart, L. L., Meyers, C. A., Smith, D. M., & Sporn, M. B. (1983) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.80.12.3676 · Cited by 398 · see citing works
The extracellular matrix of lip wounds in fetal, neonatal and adult mice
Whitby, D. J., & Ferguson, M. W. J. (1991) · Development · doi:10.1242/dev.112.2.651 · Cited by 390 · see citing works
Gorsch, S. M., Memoli, V. A., Stukel, T. A., Gold, L. I., & Arrick, B. A. (1992) · PubMed · Cited by 343 · see citing works
Pelton, R. W., Dickinson, M. E., Moses, H. L., & Hogan, B. L. M. (1990) · Development · doi:10.1242/dev.110.2.609 · Cited by 324 · see citing works
Jobling, M. F., Mott, J. D., Finnegan, M. T., Jurukovski, V., Erickson, A. C., Walian, P. J., Taylor, S. E., Ledbetter, S., Lawrence, C. M., Rifkin, D. B., et al. (2006) · Radiation Research · doi:10.1667/rr0695.1 · Cited by 300 · see citing works
Robinson, S. D., Silberstein, G. B., Roberts, A. B., Flanders, K. C., & Daniel, C. W. (1991) · Development · doi:10.1242/dev.113.3.867 · Cited by 230 · see citing works
Self-citationMeyer, A., Wang, W., Qu, J., Croft, L. B., Degen, J. L., Coller, B. S., & Ahamed, J. (2011) · Blood · doi:10.1182/blood-2011-09-377648 · Cited by 204 · see citing works
Hoyt, D. G., & Lazo, J. S. (1988) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)22161-9 · Cited by 198 · see citing works
Differential expression of genes encoding TGFs β1, β2, and β3 during murine palate formation
Pelton, R. W., Hogan, B. L. M., Miller, D. A., & Moses, H. L. (1990) · Developmental Biology · doi:10.1016/0012-1606(90)90401-4 · Cited by 192 · see citing works
The Role of Strain Variation in Murine Bleomycin-lnduced Pulmonary Fibrosis
Schrier, D. J., Kunkel, R. G., & Phan, S. H. (1983) · American Review of Respiratory Disease · doi:10.1164/arrd.1983.127.1.63 · Cited by 186 · see citing works
D’Cruz, C. M., Moody, S. E., Master, S. R., Hartman, J. L., Keiper, E. A., Imielinski, M. B., Cox, J. D., Wang, J., Ha, S. I., Keister, B. A., et al. (2002) · Molecular Endocrinology · doi:10.1210/me.2002-0073 · Cited by 175 · see citing works
Post-transcriptional regulation of the human transforming growth factor-beta 1 gene.
Kim, S. J., Park, K., Koeller, D. M., Kim, K. Y., Wakefield, L. M., Sporn, M. B., & Roberts, A. B. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)42270-3 · Cited by 172 · see citing works
Self-citationKolb, M., Bonniaud, P., Galt, T., Sime, P. J., Kelly, M. M., Margetts, P. J., & Gauldie, J. (2002) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.27.2.4674 · Cited by 168 · see citing works
The role of mouse strain differences in the susceptibility to fibrosis: a systematic review
Walkin, L., Herrick, S. E., Summers, A., Brenchley, P. E., Hoff, C. M., Korstanje, R., & Margetts, P. J. (2013) · Fibrogenesis & Tissue Repair · doi:10.1186/1755-1536-6-18 · Cited by 160 · see citing works
Wakefield, L. M., Letterio, J. J., Chen, T., Danielpour, D., Allison, R. S., Pai, L. H., Denicoff, A. M., Noone, M., Cowan, K. H., & O’Shaughnessy, J. (1995) · PubMed · Cited by 158 · see citing works
Self-citationInhibition of translation of transforming growth factor-beta 3 mRNA by its 5' untranslated region.
Arrick, B. A., Lee, A. L., Grendell, R. L., & Derynck, R. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.9.4306 · Cited by 131 · see citing works
Biomechanics of TGFβ‐induced epithelial‐mesenchymal transition: implications for fibrosis and cancer
O’Connor, J. W., & Gomez, E. W. (2014) · Clinical and Translational Medicine · doi:10.1186/2001-1326-3-23 · Cited by 131 · see citing works
Danielpour, D., Kim, K.-Y., Dart, L. L., Watanabe, S., Roberts, A. B., & Sporn, M. B. (1989) · Growth Factors · doi:10.3109/08977198909069082 · Cited by 124 · see citing works
Robertson, I. B., & Rifkin, D. B. (2013) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2013.06.003 · Cited by 113 · see citing works
4 Transforming Growth Factor-β and Its Actions on Cellular Growth and Differentiation
Nilsen‐Hamilton, M. (1990) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(08)60085-x · Cited by 104 · see citing works
Khan, S. A., Joyce, J., & Tsuda, T. (2012) · BMC Research Notes · doi:10.1186/1756-0500-5-636 · Cited by 87 · see citing works
Hawinkels, L. J. A. C., Verspaget, H. W., van Duijn, W., Zon, J. M. V. D., Zuidwijk, K., Kubben, F. J. G. M., Verheijen, J. H., Hommes, D. W., Lamers, C. B. H. W., & Sier, C. F. M. (2007) · British Journal of Cancer · doi:10.1038/sj.bjc.6603877 · Cited by 86 · see citing works
Desruisseau, S., Palmari, J., Giusti, C., Romain, S., Martin, P.-M., & Berthois, Y. (2006) · British Journal of Cancer · doi:10.1038/sj.bjc.6602920 · Cited by 86 · see citing works
Huang, T., Schor, S. L., & Hinck, A. P. (2014) · Biochemistry · doi:10.1021/bi500647d · Cited by 77 · see citing works
Kulkarni, A. B., Thyagarajan, T., & Letterio, J. J. (2002) · Current Molecular Medicine · doi:10.2174/1566524024605699 · Cited by 73 · see citing works
Flanders, K. C., & Wakefield, L. M. (2009) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-009-9122-z · Cited by 71 · see citing works
Self-citationBarcellos‐Hoff, M. H., Ehrhart, E. J., Kalia, M., Jirtle, R. L., Flanders, K. C., & Tsang, M. (1995) · Europe PMC (PubMed Central) · Cited by 65 · see citing works
Self-citationFigueroa, J. D., Flanders, K. C., García‐Closas, M., Anderson, W. F., Yang, X. R., Matsuno, R. K., Duggan, M. A., Pfeiffer, R. M., Ooshima, A., Cornelison, R., et al. (2009) · Breast Cancer Research and Treatment · doi:10.1007/s10549-009-0590-z · Cited by 60 · see citing works
Self-citationAlonso, D. F., Farias, E., Urtreger, A. J., Ladeda, V., Vidal, M., & Joffé, E. B. D. K. (1996) · Journal of Surgical Oncology · doi:10.1002/(sici)1096-9098(199608)62:4 · Cited by 58 · see citing works
Grau, A. M., Wen, W., Ramroopsingh, D. S., Gao, Y., Zi, J., Cai, Q., Shu, X., & Zheng, W. (2007) · Breast Cancer Research and Treatment · doi:10.1007/s10549-007-9845-8 · Cited by 45 · see citing works
Hall, B. E., Wankhade, U. D., Konkel, J. E., Cherukuri, K. S., Nagineni, C. N., Flanders, K. C., Arany, P. R., Chen, W., Rane, S. G., & Kulkarni, A. B. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.480764 · Cited by 42 · see citing works
Self-citationGenetic variants of Tgfb1 act as context-dependent modifiers of mouse skin tumor susceptibility
Mao, J., Saunier, E. F., de Koning, J. P., McKinnon, M. L., Higgins, M. N., Nicklas, K., Yang, H., Balmain, A., & Akhurst, R. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602581103 · Cited by 41 · see citing works
Genetic modifiers interact with maternal determinants in vascular development of Tgfb1(-/-) mice.
Tang, Y., McKinnon, M., Leong, L., Rusholme, S., Wang, S., & Akhurst, R. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg164 · Cited by 39 · see citing works
Danielpour, D., & Roberts, A. B. (1995) · Journal of Immunological Methods · doi:10.1016/0022-1759(94)00322-n · Cited by 25 · see citing works
Mammary Epithelial Transplant Procedure
Dunphy, K. A., Tao, L., & Jerry, D. J. (2010) · Journal of Visualized Experiments · doi:10.3791/1849 · Cited by 22 · see citing works
P. Hinck, A., & D. O'Connor-McCourt, M. (2011) · Current Pharmaceutical Biotechnology · doi:10.2174/138920111798808383 · Cited by 21 · cited 1× · see citing works
“Mammals express 3 highly conserved TGF-β isoforms, TGF-β1, TGF-β2, and TGF-β3, which have 70-80% identity in the amino acid sequences of their mature active domains [5].”
Angenete, E., Langenskiöld, M., Palmgren, I., Falk, P., Öresland, T., & Ivarsson, M. (2007) · International Journal of Colorectal Disease · doi:10.1007/s00384-007-0342-7 · Cited by 17 · see citing works
Riemenschneider, M. J., Hirblinger, M., Vollmann‐Zwerenz, A., Hau, P., Proescholdt, M. A., Jaschinski, F., Rothhammer-Hampl, T., Wosikowski, K., Janicot, M., & Leo, E. (2015) · Oncotarget · doi:10.18632/oncotarget.5780 · Cited by 11 · see citing works
Buehring (2004) · doi:10.1290/1543-706x(2004)40
Flagged first, then by citations
Cited by
Sorted by citations
TGFβ biology in cancer progression and immunotherapy
Derynck, R., Turley, S. J., & Akhurst, R. J. (2021) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-020-0403-1 · Cited by 944 · see citing works
Targeting TGFβ signal transduction for cancer therapy
Liu, S., Ren, J., & ten Dijke, P. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00436-9 · Cited by 413 · see citing works
“There are three highly structurally related mammalian TGFβ isoforms, that is, TGFβ1, TGFβ2, and TGFβ3.”
Knudson, K. M., Hicks, K. C., Luo, X., Chen, J.-Q., Schlom, J., & Gameiro, S. R. (2018) · OncoImmunology · doi:10.1080/2162402x.2018.1426519 · Cited by 195 · see citing works
Self-citationTGF-β uncouples glycolysis and inflammation in macrophages and controls survival during sepsis
Gauthier, T., Yao, C., Dowdy, T., Jin, W., Lim, Y.-J., Patiño, L. C., Liu, N., Ohlemacher, S. I., Bynum, A., Kazmi, R., et al. (2023) · Science Signaling · doi:10.1126/scisignal.ade0385 · Cited by 109 · see citing works
Intercellular coupling between peripheral circadian oscillators by TGF-β signaling
Finger, A., Jäschke, S., del Olmo, M., HURWITZ, R. M., Granada, A. E., Herzel, H., & Kramer, A. (2021) · Science Advances · doi:10.1126/sciadv.abg5174 · Cited by 80 · see citing works
Danielpour, D. (2024) · Pharmaceuticals · doi:10.3390/ph17040533 · Cited by 52 · see citing works
The Role of the Transforming Growth Factor-β Signaling Pathway in Gastrointestinal Cancers
Matsuoka, T., & Yashiro, M. (2023) · Biomolecules · doi:10.3390/biom13101551 · Cited by 31 · see citing works
Welsh, B. T., Faucette, R., Bilic, S., Martin, C. J., Schürpf, T., Chen, D. J., Nicholls, S. B., Lansita, J. A., & Kalra, A. V. (2021) · International Journal of Toxicology · doi:10.1177/1091581821998945 · Cited by 26 · see citing works
Taber, A. K., Konecny, A., Oda, S. K., Scott-Browne, J. P., & Prlic, M. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2313228120 · Cited by 25 · see citing works
Chang, L., Wei, Y., Qu, Y., Zhao, M., Zhou, X., Long, Y., & Hashimoto, K. (2024) · Neurobiology of Disease · doi:10.1016/j.nbd.2024.106573 · Cited by 25 · see citing works
Exploiting Canonical TGFβ Signaling in Cancer Treatment
Liu, Q., Chen, G., Moore, J., Guix, I., Placantonakis, D., & Barcellos-Hoff, M. H. (2021) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-20-0891 · Cited by 25 · see citing works
Commensal Skin Bacteria Exacerbate Inflammation and Delay Skin Barrier Repair
Khadka, V. D., Markey, L., Boucher, M., & Lieberman, T. D. (2024) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2024.03.033 · Cited by 28 · see citing works
Hoseinzadeh, A., Rezaieyazdi, Z., Mahmoudi, M., Afshari, J. T., Arab, F. L., Esmaeili, S., Faridzadeh, A., Rezaeian, A., Hoseini, S., Barati, M., et al. (2023) · International Immunopharmacology · doi:10.1016/j.intimp.2023.109699 · Cited by 23 · see citing works
Gonzàlez-Juncà, A., Reiners, O., Borrero-García, L. D., Beckford-Vera, D., Lazar, A. A., Chou, W. S., Braunstein, S. E., VanBrocklin, H. F., Franc, B. L., & Barcellos‐Hoff, M. H. (2020) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2020.09.043 · Cited by 21 · see citing works
Bojalil, R., Ruíz-Hernández, A., Villanueva-Arias, A., Amezcua-Guerra, L. M., Cásarez-Alvarado, S., Hernández-Dueñas, A. M. D. R., Rodríguez-Galicia, V., Pavón, L., Marquina, B., Becerril‐Villanueva, E., et al. (2023) · Biological Research · doi:10.1186/s40659-023-00469-8 · Cited by 19 · see citing works
Guo, H., Li, J., Wang, Y., Cao, X., Lv, X., Yang, Z., & Chen, Z. (2023) · Genes · doi:10.3390/genes14061163 · Cited by 14 · see citing works
Takahashi, M., Hashimoto, Y., & Nakamura, Y. (2022) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2022.06.001 · Cited by 13 · see citing works
Revisiting the TGFβ paradox: insights from HPV-driven cancer and the DNA damage response
Barcellos‐Hoff, M. H., & Yom, S. S. (2025) · Nature reviews. Cancer · doi:10.1038/s41568-025-00819-6 · Cited by 13 · see citing works
Transforming growth factor beta (TGF-β) activity in immuno-oncology studies
Gallo-Oller, G., Scala, M. D., Aranda, F., & Dotor, J. (2019) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2019.06.008 · Cited by 6 · see citing works
Chen, X., Liu, D., Jin, J., Yao, H., Yao, S., Liu, Y., Sun, J., & Yang, Y. (2025) · Advanced Science · doi:10.1002/advs.202506827 · Cited by 4 · see citing works
Self-citationZhang, Q., Zhang, R., Li, Y., & Yang, X. (2024) · Journal of Ovarian Research · doi:10.1186/s13048-024-01393-5 · Cited by 4 · see citing works
Commensal skin bacteria exacerbate inflammation and delay skin healingPreprint
Khadka, V. D., Markey, L., Boucher, M., & Lieberman, T. D. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.12.04.569980 · Cited by 3 · see citing works
Cai, Y., Zhu, T., Zhao, M., Xu, D., Murayama, R., Liu, G., Yue, Y., Yang, J.-J., Nakamura, H., & Hashimoto, K. (2026) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2026.178915 · Cited by 2 · see citing works
TGF-β: A silent player regulating CD8 T cell memory
Zambrano-Romero, J. D., Ríos-Ramírez, D. B., García-Rasilla, V. Y., Ruiz-Medina, B. E., & Licona-Limón, P. (2025) · Clinical Immunology · doi:10.1016/j.clim.2025.110612 · Cited by 1 · see citing works
El-Desoukey, N. A., Diaa, N., Fouad, A. A., & Maksoud, F. A. (2026) · The Egyptian Journal of Haematology · doi:10.4103/ejh.ejh_86_25 · Cited by 1 · see citing works
Carvalho, M. I., Silva-Carvalho, R., Prada, J., Pinto, C., Gregório, H., Lobo, L., Pires, I. C. R., & QUEIROGA, F. L. (2024) · Veterinary Quarterly · doi:10.1080/01652176.2024.2390941 · Cited by 1 · see citing works
Yang, Y., Yang, H. H., Tang, B., Wu, A. M. L., Flanders, K. C., Moshkovich, N., Weinberg, D. S., Welsh, M. A., Weng, J. F., Ochoa, H. J., et al. (2023) · doi:10.1158/1078-0432.22478228
Self-citationYuan, Y., Yang, H. H., Tang, B., Wu, A. M. L., Flanders, K. C., Moshkovich, N., Weinberg, D. S., Welsh, M. A., Weng, J. F., Ochoa, H. J., et al. (2023) · doi:10.1158/1078-0432.22478228.v1
Self-citationChang, R., Jia, H., Chen, Y., Loor, J. J., Xu, Q., Ma, L., Li, M., Shen, T., Li, X., Xu, C., et al. (2025) · Journal of Dairy Science · doi:10.3168/jds.2025-26828
Zhang, Q., Zhang, R., Li, Y., & Yang, X. (2024) · Figshare · doi:10.6084/m9.figshare.26698535
Zhang, Q., Zhang, R., Li, Y., & Yang, X. (2024) · Figshare · doi:10.6084/m9.figshare.26698526
Zhang, Q., Zhang, R., Li, Y., & Yang, X. (2024) · Figshare · doi:10.6084/m9.figshare.25495242
Zhang, Q., Zhang, R., Li, Y., & Yang, X. (2024) · Figshare · doi:10.6084/m9.figshare.26698529
Zhang, Q., Zhang, R., Li, Y., & Yang, X. (2024) · Figshare · doi:10.6084/m9.figshare.26698532
Zhang, Q., Zhang, R., Li, Y., & Yang, X. (2024) · Figshare · doi:10.6084/m9.figshare.25495140
The Elovl5 enzyme in breast cancer : regulation of cancer cell proliferation and metastasis
Kieu, T. (2021) · theses.fr (ABES) · doi:10.70675/09ffad1dzef26z436ez94eezf8f77c83e342
Application of tumor microenvironment targeting aptamers in cancer diagnosis and treatment
Shao, Z., Zeng, Y., He, J., Liu, X., & Tan, W. (2026) · Scientia Sinica Chimica · doi:10.1360/ssc-2025-0229
Cimino, J. L., Moshkani, S., Bailey, J. T., Rexhouse, C., Waldran, M. J., & Robek, M. D. (2026) · The Journal of Immunology · doi:10.1093/jimmun/vkag129
- Authors
- Flanders, K. C., Yang, Y.-A., Herrmann, M., Chen, J., Mendoza, N., Mirza, A. M., & Wakefield, L. M.
- Affiliations
- National Institutes of Health (US)
- Laboratory of Cancer Biology and Genetics, National Cancer Institute, Bethesda, Maryland, United States of America
- XOMA (United States) (US)
- Corresponding author
- Flanders, Kathleen C.
- Yang, Yu-an
- Venue
- Oncotarget
- Publisher
- Impact Journals, LLC
- Published
- 2016-05-17
- Volume
- 7
- Issue
- 25
- Pages
- 38164-38179
- ISSN
- 1949-2553 (ISSN-L)
- PMC
- PMC5122380
- OpenAlex
- W2404501987
- Cited by
- 39
- References
- 65
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 11 · 2023: 9 · 2022: 2 · 2021: 5 · 2020: 2 · 2019: 1 · 2018: 1
- FWCI
- 0.35
- Type
- journal article
- Language
- en
- Open access
- diamond
- doi.org
- Licence
- cc-by
- Locations
- Oncotarget (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Cancer Institute (ZIABC010881)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Health Sciences › Medicine › Oncology › HER2/EGFR in Cancer Research
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Keywords
- TGF-beta isoforms, TGF-β1, TGF-beta2, TGF-beta3, mammary gland, mammary carcinogenesis, mammary epithelium, protein quantification, tissue-specific gene expression, mouse strains, luminal epithelium
- MeSH terms
- Animals, Female, Humans, Mammary Neoplasms, Experimental, Mice, Inbred BALB C, Transforming Growth Factor beta, Protein Isoforms, Mice, Transforming Growth Factor beta1, Transforming Growth Factor beta3
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