Targeting the TGFβ signalling pathway in disease

Akhurst, Rosemary J.; Hata, Akiko

doi:10.1038/nrd3810

Cited by 1,466TGF-β signaling in diseasesConnective tissue disorders researchLiver physiology and pathology

Targeting the TGFβ signalling pathway in disease

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Akhurst, Rosemary J., Hata, Akiko·2012·Nature Reviews Drug Discovery

DOI 10.1038/nrd3810PMC PMC3520610

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Abstract

Many drugs that target transforming growth factor-β (TGFβ) signalling have been developed, some of which have reached Phase III clinical trials for a number of disease applications. Preclinical and clinical studies indicate the utility of these agents in fibrosis and oncology, particularly in augmentation of existing cancer therapies, such as radiation and chemotherapy, as well as in tumour vaccines. There are also reports of specialized applications, such as the reduction of vascular symptoms of Marfan syndrome. Here, we consider why the TGFβ signalling pathway is a drug target, the potential clinical applications of TGFβ inhibition, the issues arising with anti-TGFβ therapy and how these might be tackled using personalized approaches to dosing, monitoring of biomarkers as well as brief and/or localized drug-dosing regimens.

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Systemic TGF-β blockade was associated with immune dysregulation, impaired tissue homeostasis, and increased oncogenic risk, limiting broader clinical application.
“these studies also highlighted the limitations of systemic pathway inhibition as systemic TGF-β blockade was associated with immune dysregulation, impaired tissue homeostasis, and increased oncogenic risk, limiting broader clinical application (141).”
From Targeting macrophages in liver fibrosis (2026) · cites this paper as [141]
The Cancer section identifies inflammation, autoimmunity, cardiovascular defects and loss of tumour suppression as concerns with TGF-β inhibition; it also reports increased metastases in mouse models and skin lesions in one Phase I trial. But it says clinical trials had shown no widespread inflammatory complications or the cited cardiovascular and bone effects. The claim overstates these potential and preclinical risks as an established association of systemic blockade across clinical use. (LLM, conf=0.88)
Experimental — accuracy not yet measured
GDF10 signals through TGFβ receptors.
“and signals through TGFβ receptors (TGFβR)14,15.”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [14]
The TGFβ family section identifies GDFs as members of the TGFβ superfamily, and the TGFβ signalling section says members signal through type I and type II receptor complexes. The paper does not identify GDF10 specifically or establish that it uses the receptors denoted TGFβR in the citing sentence. (LLM, conf=0.82)
Experimental — accuracy not yet measured
GDF10 is a divergent member of the bone morphogenetic protein (BMP)/transforming growth factor-β (TGFβ) superfamily.
“GDF10 is a divergent member of the bone morphogenetic protein (BMP)/transforming growth factor-β (TGFβ) superfamily11–14”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [14]
The TGFβ family section identifies GDFs and BMPs as members of the TGFβ superfamily. It does not identify GDF10 specifically or describe it as divergent; searches for “GDF10” and “BMP-3b” found no such passage. Page numbers are unavailable in our copy. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Though TGF and GDF10 both signal through TGFβRI/II, their signaling levels are not equivalent.
“Though TGF and GDF10 both signal through TGFβRI/II12–14, we show that their signaling levels are not equivalent.”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [14]
The TGFβ signalling section says that TGFβ-superfamily ligands signal through type I and type II receptors, and The TGFβ family section includes GDFs in that superfamily (page numbers unavailable). It does not establish that GDF10 specifically uses TGFβRI/II. The difference in signalling levels is presented as the citing authors’ own finding, not as a claim attributed to this source. (LLM, conf=0.83)
Experimental — accuracy not yet measured
Such context-specific signaling is a hallmark of TGFβ in its role in cancer, where it switches from inhibition of tumor growth and metastasis to promotion of endothelial to mesenchymal transition and metastasis as the local tumor environment evolves.
“Such context-specific signaling is a hallmark of TGFβ in its role in cancer, where it switches from inhibition of tumor growth and metastasis to promotion of endothelial to mesenchymal transition and metastasis as the local tumor environment evolves14,43.”
From GDF10 is a signal for axonal sprouting and functional recovery after stroke (2015) · cites this paper as [14]
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Small Molecular Inhibitor of Transforming Growth Factor-β Protects Against Development of Radiation-Induced Lung Injury
Anscher, M. S., Thrasher, B. A., Zgonjanin, L., Rabbani, Z. N., Corbley, M. J., Fu, K., Sun, L., Lee, W., Ling, L. E., & Vujašković, Ž. (2008) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2008.02.046 · Cited by 133 · see citing works
Targeted inhibition of activin receptor-like kinase 5 signaling attenuates cardiac dysfunction following myocardial infarction
Tan, S. M., Zhang, Y., Connelly, K. A., Gilbert, R. E., & Kelly, D. J. (2010) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01048.2009 · Cited by 130 · see citing works
Inhibition of transforming growth factor β receptor I kinase blocks hepatocellular carcinoma growth through neo‐angiogenesis regulation
Mazzocca, A., Fransvea, E., Lavezzari, G., Antonaci, S., & Giannelli, G. (2009) · Hepatology · doi:10.1002/hep.23118 · Cited by 127 · see citing works
PiggyBac-mediated Cancer Immunotherapy Using EBV-specific Cytotoxic T-cells Expressing HER2-specific Chimeric Antigen Receptor
Nakazawa, Y., Huye, L. E., Salsman, V. S., et al. (2011) · Molecular Therapy · doi:10.1038/mt.2011.131 · Cited by 127 · see citing works
Signaling cross-talk between TGF-β/BMP and other pathways
Xing, Guo, Xiaofan, & Wang (2009) · Cell Research · Cited by 125 · see citing works
A synthetic peptide from transforming growth factor β type III receptor inhibits liver fibrogenesis in rats with carbon tetrachloride liver injury
Ezquerro, I.-J., Lasarte, J. J., Dotor, J., Castilla‐Cortázar, I., Bustos, M., Peñuelas, I., Blanco, G., Rodríguez‐Ortigosa, C. M., Lechuga, M. D. C. G., Greenwel, P., et al. (2003) · Cytokine · doi:10.1016/s1043-4666(03)00101-7 · Cited by 123 · see citing works
Skin Tumors Induced by Sorafenib; Paradoxic RAS–RAF Pathway Activation and Oncogenic Mutations of HRAS , TP53 , and TGFBR1
Arnault, J. P., Mateus, C., Escudier, B. J., et al. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-1344 · Cited by 123 · see citing works
Anti–Transforming Growth Factor β Receptor II Antibody Has Therapeutic Efficacy against Primary Tumor Growth and Metastasis through Multieffects on Cancer, Stroma, and Immune Cells
Zhong, Z., Carroll, K. D., Policarpio, D., Osborn, C., Gregory, M., Bassi, R., Jimenez, X., Prewett, M., Liebisch, G., Persaud, K., et al. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-1634 · Cited by 123 · see citing works
Expression of αvβ8 integrin on dendritic cells regulates Th17 cell development and experimental autoimmune encephalomyelitis in mice
Melton, A. C., Bailey-Bucktrout, S. L., Travis, M. A., Fife, B. T., Bluestone, J. A., & Sheppard, D. (2010) · Journal of Clinical Investigation · doi:10.1172/jci43786 · Cited by 123 · see citing works
TGF-β antagonists: Why suppress a tumor suppressor?
Akhurst, R. J. (2002) · Journal of Clinical Investigation · doi:10.1172/jci15970 · Cited by 120 · see citing works
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Immunotherapy targeting HER2 with genetically modified T cells eliminates tumor-initiating cells in osteosarcoma
Rainusso, N., Brawley, V. S., Ghazi, A., Hicks, M. J., Gottschalk, S., Rosen, J. M., & Ahmed, N. (2012) · Cancer Gene Therapy · doi:10.1038/cgt.2011.83 · Cited by 114 · see citing works
A Novel Small-Molecule Inhibitor of Transforming Growth Factor β Type I Receptor Kinase (SM16) Inhibits Murine Mesothelioma Tumor Growth In vivo and Prevents Tumor Recurrence after Surgical Resection
Suzuki, E., Kim, S., Cheung, H.-K., Corbley, M. J., Zhang, X., Sun, L., Shan, F., Singh, J., Lee, W.-C., Albelda, S. M., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-2389 · Cited by 113 · see citing works
TGF Beta Inhibition for Cancer Therapy
Saunier, E. F., & Akhurst, R. J. (2006) · Current Cancer Drug Targets · doi:10.2174/156800906778742460 · Cited by 112 · see citing works
Self-citation
Transforming Growth Factor β Receptor I Kinase Inhibitor Down-Regulates Cytokine Secretion and Multiple Myeloma Cell Growth in the Bone Marrow Microenvironment
Hayashi, T., Hideshima, T., Nguyen, A. N., Munoz, O., Podar, K., Hamasaki, M., Ishitsuka, K., Yasui, H., Richardson, P., Chakravarty, S., et al. (2004) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-04-0632 · Cited by 110 · see citing works
Discovery of 4-{4-[3-(Pyridin-2-yl)-1H-pyrazol-4-yl]pyridin-2-yl}-N-(tetrahydro-2H- pyran-4-yl)benzamide (GW788388): A Potent, Selective, and Orally Active Transforming Growth Factor-β Type I Receptor Inhibitor
Gellibert, F. J., de Gouville, A., Woolven, J. M., Mathews, N., Nguyen, V.-L., Ruault, C., Patikis, A. N., Grygielko, E. T., Laping, N. J., & Huet, S. (2006) · Journal of Medicinal Chemistry · doi:10.1021/jm0509905 · Cited by 107 · see citing works
A synthetic peptide from transforming growth factor- 1 type III receptor prevents myocardial fibrosis in spontaneously hypertensive rats
Hermida, N., López, B., González, A., Dotor, J., Lasarte, J. J., Sarobe, P., Borrás‐Cuesta, F., & Dı́ez, J. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn315 · Cited by 107 · see citing works
TGF-β antagonists: Why suppress a tumor suppressor?
Akhurst, R. J. (2002) · Journal of Clinical Investigation · doi:10.1172/jci0215970 · Cited by 107 · see citing works
Self-citation
Few Smad proteins and many Smad-interacting proteins yield multiple functions and action modes in TGFβ/BMP signaling in vivo
Conidi, A., Cazzola, S., Beets, K., Coddens, K., Collart, C., Cornelis, F. M. F., Cox, L., Debruyn, J., Dobreva, M. P., Dries, R., et al. (2011) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2011.11.006 · Cited by 103 · see citing works
Epigenetic downregulation of human disabled homolog 2 switches TGF-β from a tumor suppressor to a tumor promoter
Hannigan, A., Smith, P., Kalna, G., Nigro, C. L., Orange, C., O’Brien, D. I., Shah, R., Syed, N., Spender, L. C., Herrera, B. M., et al. (2010) · Journal of Clinical Investigation · doi:10.1172/jci36125 · Cited by 102 · see citing works
Gene transfer of Smad7 using electroporation of adenovirus prevents renal fibrosis in post-obstructed kidney
Terada, Y., Hanada, S., Nakao, A., Kuwahara, M., Sasaki, S., & Marumo, F. (2002) · Kidney International · doi:10.1046/j.1523-1755.2002.0610s1094.x · Cited by 101 · see citing works
Transforming Growth Factor-β Can Suppress Tumorigenesis through Effects on the Putative Cancer Stem or Early Progenitor Cell and Committed Progeny in a Breast Cancer Xenograft Model
Tang, B., Yoo, N., Vu, M. A., Mamura, M., Nam, J., Ooshima, A., Du, Z., Desprez, P. Y., Anver, M. R., Michalowska, A. M., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-0982 · Cited by 99 · see citing works
Transforming growth factor β (TGFβ)-induced apoptosis: The rise and fall of Bim
Ramesh, S., Wildey, G. M., & Howe, P. H. (2009) · Cell Cycle · doi:10.4161/cc.8.1.7291 · Cited by 97 · see citing works
Rapamycin Potentiates Transforming Growth Factor β-Induced Growth Arrest in Nontransformed, Oncogene-Transformed, and Human Cancer Cells
Law, B. K., Chytil, A. M., Dumont, N., Hamilton, E. G., Waltner-Law, M. E., Aakre, M. E., Covington, C. D., & Moses, H. L. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.23.8184-8198.2002 · Cited by 97 · see citing works
The TGF-β Family
Derynck, R., & 宮園, 浩. (2008) · Cold Spring Harbor Laboratory eBooks · Cited by 96 · see citing works
Activin/TGFβ and BMP crosstalk determines digit chondrogenesis
Montero, J. A., Lorda-Diez, C. I., Gañán, Y., et al. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.06.022 · Cited by 95 · see citing works
Mad Upregulation and Id2 Repression Accompany Transforming Growth Factor (TGF)-β-mediated Epithelial Cell Growth Suppression
Siegel, P. M., Shu, W., & Massagué, J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301413200 · Cited by 95 · see citing works
Blockade of TSP1-Dependent TGF-β Activity Reduces Renal Injury and Proteinuria in a Murine Model of Diabetic Nephropathy
Lu, A., Miao, M., Schoeb, T. R., Agarwal, A., & Murphy-Ullrich, J. E. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2011.02.039 · Cited by 92 · see citing works
αv Integrin expression by DCs is required for Th17 cell differentiation and development of experimental autoimmune encephalomyelitis in mice
Acharya, M., Mukhopadhyay, S., Païdassi, H., Jamil, T., Chow, C., Kissler, S., Stuart, L. M., Hynes, R. O., & Lacy‐Hulbert, A. (2010) · Journal of Clinical Investigation · doi:10.1172/jci43796 · Cited by 91 · see citing works
N-[3,4-dimethoxycinnamoyl]-anthranilic acid (tranilast) inhibits transforming growth factor-? release and reduces migration and invasiveness of human malignant glioma cells
Platten, M., Wild‐Bode, C., Wick, W., Leitlein, J., DICHGANS, J., & Weller, M. (2001) · International Journal of Cancer · doi:10.1002/ijc.1289 · Cited by 89 · see citing works
Mutations of TGFß signaling molecules in human disease
Harradine, K. A., & Akhurst, R. J. (2006) · Annals of Medicine · doi:10.1080/07853890600919911 · Cited by 87 · see citing works
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Antisense Therapeutics for Tumor Treatment: The TGF-beta2 Inhibitor AP 12009 in Clinical Development Against Malignant Tumors
Schlingensiepen, K., Fischer-Blass, B., Schmaus, S., & Ludwig, S. (2007) · Recent results in cancer research/Recent Results in Cancer Research · doi:10.1007/978-3-540-71279-4_16 · Cited by 86 · see citing works
Discovery and development of avotermin (recombinant human transforming growth factor beta 3): A new class of prophylactic therapeutic for the improvement of scarring
Occleston, N. L., O’Kane, S., Laverty, H., Cooper, M., Fairlamb, D. M., Mason, T., Bush, J. A., & Ferguson, M. W. J. (2011) · Wound Repair and Regeneration · doi:10.1111/j.1524-475x.2011.00711.x · Cited by 86 · see citing works
Bone Sialoprotein Mediates the Tumor Cell–Targeted Prometastatic Activity of Transforming Growth Factor β in a Mouse Model of Breast Cancer
Nam, J., Suchar, A. M., Kang, M., Stuelten, C. H., Tang, B., Michalowska, A. M., Fisher, L. W., Fedarko, N. S., Jain, A., Pinkas, J., et al. (2006) · Cancer Research · doi:10.1158/0008-5472.can-06-0068 · Cited by 85 · see citing works
SM16, an Orally Active TGF-β Type I Receptor Inhibitor Prevents Myofibroblast Induction and Vascular Fibrosis in the Rat Carotid Injury Model
Fu, K., Corbley, M. J., Sun, L., Friedman, J. E., Shan, F., Papadatos, J. L., Costa, D. E., Lutterodt, F., Sweigard, H., Bowes, S., et al. (2008) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.107.158030 · Cited by 85 · see citing works
Transforming Growth Factor-β Receptor Blockade Augments the Effectiveness of Adoptive T-Cell Therapy of Established Solid Cancers
Wallace, A. F., Kapoor, V., Sun, J., Mrass, P., Weninger, W., Heitjan, D. F., June, C. H., Kaiser, L. R., Ling, L. E., & Albelda, S. Μ. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-0356 · Cited by 84 · see citing works
Searching for MiR-acles in Cardiac Fibrosis
van Rooij, E., & Olson, E. N. (2009) · Circulation Research · doi:10.1161/circresaha.108.192492 · Cited by 84 · see citing works
Systemic Blockade of Transforming Growth Factor-β Signaling Augments the Efficacy of Immunogene Therapy
Kim, S., Buchlis, G., Fridlender, Z. G., Sun, J., Kapoor, V., Cheng, G., Haas, A. R., Cheung, H. K., Zhang, X., Corbley, M. J., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-1494 · Cited by 84 · see citing works
Antibody Targeting of TGF-β in Cancer Patients
Lonning, S. M., Mannick, J. B., & McPherson, J. M. (2011) · Current Pharmaceutical Biotechnology · doi:10.2174/138920111798808392 · Cited by 84 · see citing works
Blockade of Tumor Cell Transforming Growth Factor-βs Enhances Cell Cycle Progression and Sensitizes Human Breast Carcinoma Cells to Cytotoxic Chemotherapy
Ohmori, T., Yang, J.-L., Price, J. O., & Arteaga, C. L. (1998) · Experimental Cell Research · doi:10.1006/excr.1998.4261 · Cited by 83 · see citing works
Outgrowth of Drug-Resistant Carcinomas Expressing Markers of Tumor Aggression after Long-term TβRI/II Kinase Inhibition with LY2109761
Connolly, E. C., Saunier, E. F., Quigley, D., Luu, M. T., De Sapio, A., Hann, B., Yingling, J. M., & Akhurst, R. J. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-2941 · Cited by 82 · see citing works
Self-citation
Transforming growth factor-β decreases the cancer-initiating cell population within diffuse-type gastric carcinoma cells
Ehata, S., Johansson, E., Katayama, R., Koike, S., Watanabe, A., Hoshino, Y., Katsuno, Y., Komuro, A., Koinuma, D., Kano, M. R., et al. (2010) · Oncogene · doi:10.1038/onc.2010.546 · Cited by 81 · see citing works
Acute development of multiple keratoacanthomas and squamous cell carcinomas after treatment with infliximab
Esser, A. C., Abril, A., Fayne, S., & Doyle, J. A. (2004) · Journal of the American Academy of Dermatology · doi:10.1016/j.jaad.2003.11.044 · Cited by 80 · see citing works
Extended adjuvant temozolomide for treatment of newly diagnosed glioblastoma multiforme
Urgoiti, G. B. R., Singh, A. D., & Easaw, J. C. (2012) · Journal of Neuro-Oncology · doi:10.1007/s11060-012-0826-3 · Cited by 78 · see citing works
The clinical significance of 5% change in vital capacity in patients with idiopathic pulmonary fibrosis: extended analysis of the pirfenidone trial
Taniguchi, H., Kondoh, Y., Ebina, M., Azuma, A., Ogura, T., Taguchi, Y., Suga, M., Takahashi, H., Nakata, K., Sato, A., et al. (2011) · Respiratory Research · doi:10.1186/1465-9921-12-93 · Cited by 78 · see citing works
Phase I/II study of GC1008: A human anti-transforming growth factor-beta (TGFβ) monoclonal antibody (MAb) in patients with advanced malignant melanoma (MM) or renal cell carcinoma (RCC)
Morris, J. C., Shapiro, G. I., Tan, A. R., Lawrence, D. P., Olencki, T. E., Dezube, B. J., Hsu, F. J., Reiss, M., & Berzofsky, J. A. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2008.26.15_suppl.9028 · Cited by 78 · see citing works
Therapeutic effect of a peptide inhibitor of TGF-β on pulmonary fibrosis
Arribillaga, L., Dotor, J., Basagoiti, M., et al. (2010) · Cytokine · doi:10.1016/j.cyto.2010.11.019 · Cited by 71 · see citing works
Intracerebral and Intrathecal Infusion of the TGF-β2-Specific Antisense Phosphorothioate Oligonucleotide AP 12009 in Rabbits and Primates: Toxicology and Safety
Schlingensiepen, R., Goldbrunner, M., Szyrach, M., Stauder, G., Jachimczak, P., Bogdahn, U., Schulmeyer, F. J., Hau, P., & Schlingensiepen, K. (2005) · Oligonucleotides · doi:10.1089/oli.2005.15.94 · Cited by 69 · see citing works
Mouse and human strategies identify PTPN14 as a modifier of angiogenesis and hereditary haemorrhagic telangiectasia
Benzinou, M., Clermont, F. F., Letteboer, T. G. W., Kim, J.-H., Espejel, S., Harradine, K. A., Arbelaez, J., Luu, M. T., Roy, R., Quigley, D. A., et al. (2012) · Nature Communications · doi:10.1038/ncomms1633 · Cited by 67 · see citing works
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The paradoxical TGF-β vasculopathies
Akhurst, R. J. (2012) · Nature Genetics · doi:10.1038/ng.2366 · Cited by 66 · see citing works
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TGF-β signalling-related markers in cancer patients with bone metastasis
Baselga, J. M., Rothenberg, M. L., Tabernero, J. M., Seoane, J., Daly, T. M., Cleverly, A., Berry, B., Kloeker, S., RAY, C. A., Fill, J. A., et al. (2008) · Biomarkers · doi:10.1080/13547500701676019 · Cited by 66 · see citing works
Large- and small-molecule inhibitors of transforming growth factor-beta signaling.
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The Molecular Signatures Database Hallmark Gene Set Collection
Liberzon, A., Birger, C., Thorvaldsdóttir, H., Ghandi, M., Mesirov, J. P., & Tamayo, P. (2015) · Cell Systems · doi:10.1016/j.cels.2015.12.004 · Cited by 13,807 · see citing works
In situ immune response and mechanisms of cell damage in central nervous system of fatal cases microcephaly by Zika virus
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EMT, CSCs, and drug resistance: the mechanistic link and clinical implications
Shibue, T., & Weinberg, R. A. (2017) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2017.44 · Cited by 2,539 · see citing works
Molecular and cellular mechanisms of liver fibrosis and its regression
Kisseleva, T., & Brenner, D. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-020-00372-7 · Cited by 2,024 · see citing works
Age and Age-Related Diseases: Role of Inflammation Triggers and Cytokines
Rea, I. M., Gibson, D. S., McGilligan, V., McNerlan, S. E., Alexander, H. D., & Ross, O. A. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00586 · Cited by 1,267 · see citing works
Targeting TGF-β Signaling in Cancer
Colak, S., & ten Dijke, P. (2017) · Trends in cancer · doi:10.1016/j.trecan.2016.11.008 · Cited by 1,003 · see citing works
TGFβ biology in cancer progression and immunotherapy
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GFRAL is the receptor for GDF15 and the ligand promotes weight loss in mice and nonhuman primates
Mullican, S. E., Lin-Schmidt, X., Chin, C.-N., Chavez, J. A., Furman, J. L., Armstrong, A. A., Beck, S. C., South, V. J., Dinh, T. Q., Cash-Mason, T. D., et al. (2017) · Nature Medicine · doi:10.1038/nm.4392 · Cited by 774 · see citing works
Signaling Receptors for TGF-β Family Members
Heldin, C.-H., & Moustakas, A. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a022053 · Cited by 711 · see citing works
Mechanisms of Organ Injury and Repair by Macrophages
Vannella, K. M., & Wynn, T. A. (2017) · Annual Review of Physiology · doi:10.1146/annurev-physiol-022516-034356 · Cited by 656 · see citing works
IL-11 is a crucial determinant of cardiovascular fibrosis
Schafer, S., Viswanathan, S., Widjaja, A. A., Lim, W.-W., Moreno-Moral, A., DeLaughter, D. M., Ng, B., Patone, G., Chow, K., Khin, E., et al. (2017) · Nature · doi:10.1038/nature24676 · Cited by 639 · see citing works
Targeting extracellular matrix stiffness to attenuate disease: from molecular mechanisms to clinical trials
Lampi, M. C., & Reinhart-King, C. A. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aao0475 · Cited by 551 · see citing works
TGF-β Signaling in Control of Cardiovascular Function
Goumans, M.-J., & ten Dijke, P. (2018) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a022210 · Cited by 360 · see citing works
Targeting the TGFβ pathway with galunisertib, a TGFβRI small molecule inhibitor, promotes anti-tumor immunity leading to durable, complete responses, as monotherapy and in combination with checkpoint blockade
Holmgaard, R. B., Schaer, D. A., Li, Y., Castaneda, S. P., Murphy, M. Y., Xu, X., Inigo, I., Dobkin, J., Manro, J. R., Iversen, P. W., et al. (2018) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-018-0356-4 · Cited by 356 · see citing works
TGF-beta in CAF-mediated tumor growth and metastasis
Calon, A., Tauriello, D. V. F., & Batlle, E. (2014) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2013.12.008 · Cited by 342 · see citing works
Communication between EMT and PD-L1 signaling: New insights into tumor immune evasion
Jiang, Y., & Zhan, H. (2020) · Cancer Letters · doi:10.1016/j.canlet.2019.10.013 · Cited by 319 · see citing works
Myostatin/activin pathway antagonism: molecular basis and therapeutic potential
Han, H. Q., Zhou, X., Mitch, W. E., & Goldberg, A. L. (2013) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2013.05.019 · Cited by 314 · see citing works
Utilizing graph machine learning within drug discovery and development
Gaudelet, T., Day, B., Jamasb, A. R., Soman, J., Regep, C., Liu, G., Hayter, J. B. R., Vickers, R., Roberts, C., Tang, J., et al. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab159 · Cited by 313 · see citing works
TRPV4 mediates myofibroblast differentiation and pulmonary fibrosis in mice
Rahaman, S. O., Grove, L. M., Paruchuri, S., Southern, B. D., Abraham, S., Niese, K. A., Scheraga, R. G., Ghosh, S., Thodeti, C. K., Zhang, D. X., et al. (2014) · Journal of Clinical Investigation · doi:10.1172/jci75331 · Cited by 310 · see citing works
Tumor cell plasticity in targeted therapy-induced resistance: Mechanisms and new strategies
Shi, Z.-D., Pang, K., Wu, Z.-X., Dong, Y., Hao, L., Qin, J.-X., Wang, W., Chen, Z.-S., & Han, C.-H. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01383-x · Cited by 256 · see citing works
Micropeptide CIP2A-BP encoded by LINC00665 inhibits triple-negative breast cancer progression
Guo, B., Wu, S., Zhu, X., Zhang, L., Deng, J., Li, F., Wang, Y., Zhang, S., Wu, R., Lu, J., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2019102190 · Cited by 243 · see citing works
Transforming growth factor β as regulator of cancer stemness and metastasis
Bellomo, C., Caja, L., & Moustakas, A. (2016) · British Journal of Cancer · doi:10.1038/bjc.2016.255 · Cited by 235 · see citing works
TGF-&beta; signaling in cancer metastasis
Xie, F., Ling, L., Van Dam, H., Zhou, F., & Zhang, L. (2018) · Acta Biochimica et Biophysica Sinica · doi:10.1093/abbs/gmx123 · Cited by 231 · see citing works
Carcinoma‐associated fibroblasts: Non‐neoplastic tumour‐promoting mesenchymal cells
Polanska, U. M., & Orimo, A. (2013) · Journal of Cellular Physiology · doi:10.1002/jcp.24347 · Cited by 208 · see citing works
Treatment of sporadic inclusion body myositis with bimagrumab
Amato, A. A., Sivakumar, K., Goyal, N., David, W. S., Salajegheh, M., Praestgaard, J., Lach-Trifilieff, E., Trendelenburg, A.-U., Laurent, D., Glass, D. J., et al. (2014) · Neurology · doi:10.1212/wnl.0000000000001070 · Cited by 210 · see citing works
Exploration of a potent PI3 kinase/mTOR inhibitor as a novel anti-fibrotic agent in IPF
Mercer, P. F., Woodcock, H. V., Eley, J. D., Platé, M., Sulikowski, M. G., Durrenberger, P. F., Franklin, L., Nanthakumar, C. B., Man, Y., Genovese, F., et al. (2016) · Thorax · doi:10.1136/thoraxjnl-2015-207429 · Cited by 206 · see citing works
Preclinical assessment of galunisertib (LY2157299 monohydrate), a first‐in‐class transforming growth factor‐β receptor type I inhibitor
Yingling, J. M., McMillen, W. T., Yan, L., Huang, H., Sawyer, J. S., Graff, J., Clawson, D. K., Britt, K. S., Anderson, B. D., Beight, D. W., et al. (2018) · Oncotarget · doi:10.18632/oncotarget.23795 · Cited by 187 · see citing works
GDF10 is a signal for axonal sprouting and functional recovery after stroke
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Authors: Akhurst, R. J., & Hata, A.
Affiliations: University of California, San Francisco (US)
Corresponding author: Akhurst, Rosemary J.
ORCID: Akhurst, Rosemary J.
Hata, Akiko
Venue: Nature Reviews Drug Discovery
Publisher: Springer Science and Business Media LLC
Published: 2012-09-24
Volume: 11
Issue: 10
Pages: 790-811
ISSN: 1474-1776 (ISSN-L)
1474-1784
DOI: 10.1038/nrd3810
PMC: PMC3520610
OpenAlex: W2150548551
Cited by: 1,466
References: 244
Citations by year: 2026: 57 · 2025: 86 · 2024: 95 · 2023: 110 · 2022: 98 · 2021: 106 · 2020: 131 · 2019: 137 · 2018: 125 · 2017: 136 · 2016: 125 · 2015: 95 · 2014: 96 · 2013: 66 · 2012: 2
FWCI: 7.59
Type: journal article
Language: en
Update notices: erratum (2012-10-19)
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Reviews Drug Discovery (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: National Institutes of Health (5r01hl078564-05)
National Heart, Lung, and Blood Institute (R01HL108317, R01-HL078564)
National Cancer Institute (R01CA116019, R21CA164772, P30CA082103)
National Institute of General Medical Sciences (R01GM060514)
National Institute of Arthritis and Musculoskeletal and Skin Diseases (P01AR050440)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Connective tissue disorders research
Health Sciences › Medicine › Hepatology › Liver physiology and pathology
Keywords: drug development, fibrosis, cancer, inflammation, radiosensitization, chemosensitization, cancer vaccines, Marfan syndrome, individualized dosing, biomarker monitoring, local drug delivery
MeSH terms: Animals, Humans, Protein Binding, Signal Transduction, Transforming Growth Factor beta, Drug Delivery Systems, Receptors, Transforming Growth Factor beta

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Targeting the TGFβ signalling pathway in disease

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