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Roles of TGF-β in cancer hallmarks and emerging onco-therapeutic design

Published online by Cambridge University Press:  08 November 2022

Xiaofeng Dai*
Affiliation:
Wuxi School of Medicine, Jiangnan University, Wuxi 214122, China
Dong Hua
Affiliation:
Wuxi People's Hospital of Nanjing Medical University, Wuxi 21411, China
Xiaoxia Lu*
Affiliation:
Department of Oncology, Affiliated Hospital of Yangzhou University, Yangzhou 225000, China
*
Authors for correspondence: Xiaofeng Dai, E-mail: xiaofeng.dai@jiangnan.edu.cn; Xiaoxia Lu, E-mail: 091036@yzu.edu.cn
Authors for correspondence: Xiaofeng Dai, E-mail: xiaofeng.dai@jiangnan.edu.cn; Xiaoxia Lu, E-mail: 091036@yzu.edu.cn

Abstract

Transforming growth factor-beta (TGF-β) is a double-edged sword in cancer treatment because of its pivotal yet complex and roles played during cancer initiation/development. Current anti-cancer strategies involving TGF-β largely view TGF-β as an onco-therapeutic target that not only substantially hinders its full utilisation for cancer control, but also considerably restricts innovations in this field. Thereby, how to take advantages of therapeutically favourable properties of TGF-β for cancer management represents an interesting and less investigated problem. Here, by categorising cancer hallmarks into four critical transition events and one enabling characteristic controlling cancer initiation and progression, and delineating TGF-β complexities according to these cancer traits, we identify the suppressive role of TGF-β in tumour initiation and early-stage progression and its promotive functionalities in cancer metastasis as well as other cancer hallmarks. We also propose the feasibility and possible scenarios of combining cold atmospheric plasma (CAP) with onco-therapeutics utilising TGF-β for cancer control given the intrinsic properties of CAP against cancer hallmarks.

Type
Review
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Dagenais, GR et al. (2020) Variations in common diseases, hospital admissions, and deaths in middle-aged adults in 21 countries from five continents (PURE): a prospective cohort study. The Lancet 395, 785794.CrossRefGoogle ScholarPubMed
Sung, H et al. (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA: A Cancer Journal for Clinicians 71, 209249.Google ScholarPubMed
Derynck, R, Turley, SJ and Akhurst, RJ (2021) TGFbeta biology in cancer progression and immunotherapy. Nature Reviews. Clinical Oncology 18, 934.CrossRefGoogle ScholarPubMed
McPherron, AC, Lawler, AM and Lee, SJ (1997) Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387, 8390.CrossRefGoogle ScholarPubMed
Viel, S et al. (2016) TGF-beta inhibits the activation and functions of NK cells by repressing the mTOR pathway. Science Signaling 9, ra19.CrossRefGoogle ScholarPubMed
Gal, A et al. (2008) Sustained TGF beta exposure suppresses Smad and non-Smad signalling in mammary epithelial cells, leading to EMT and inhibition of growth arrest and apoptosis. Oncogene 27, 12181230.CrossRefGoogle ScholarPubMed
Moon, JR et al. (2019) TGF-beta1 protects colon tumor cells from apoptosis through XAF1 suppression. International Journal of Oncology 54, 21172126.Google ScholarPubMed
Teicher, BA (2021) TGFbeta-directed therapeutics: 2020. Pharmacology & Therapeutics 217, 107666.CrossRefGoogle ScholarPubMed
Melisi, D et al. (2019) TGFbeta receptor inhibitor galunisertib is linked to inflammation- and remodeling-related proteins in patients with pancreatic cancer. Cancer Chemotherapy and Pharmacology 83, 975991.CrossRefGoogle ScholarPubMed
Tolcher, AW et al. (2017) A phase 1 study of anti-TGFbeta receptor type-II monoclonal antibody LY3022859 in patients with advanced solid tumors. Cancer Chemotherapy and Pharmacology 79, 673680.CrossRefGoogle ScholarPubMed
Tarhini, AA et al. (2012) Safety and efficacy of combination immunotherapy with interferon alfa-2b and tremelimumab in patients with stage IV melanoma. Journal of Clinical Oncology 30, 322328.CrossRefGoogle ScholarPubMed
Sckisel, GD et al. (2015) Out-of-sequence signal 3 paralyzes primary CD4(+) T-cell-dependent immunity. Immunity 43, 240250.CrossRefGoogle ScholarPubMed
Lee, J, Choi, JH and Joo, CK (2013) TGF-beta1 regulates cell fate during epithelial-mesenchymal transition by upregulating survivin. Cell Death & Disease 4, e714.CrossRefGoogle ScholarPubMed
Sorre, B et al. (2014) Encoding of temporal signals by the TGF-beta pathway and implications for embryonic patterning. Developmental Cell 30, 334342.CrossRefGoogle ScholarPubMed
Lyon, M, Rushton, G and Gallagher, JT (1997) The interaction of the transforming growth factor-betas with heparin/heparan sulfate is isoform-specific. Journal of Biological Chemistry 272, 18000–6.CrossRefGoogle ScholarPubMed
Shi, M et al. (2011) Latent TGF-beta structure and activation. Nature 474, 343349.CrossRefGoogle ScholarPubMed
Hyytiainen, M, Penttinen, C and Keski-Oja, J (2004) Latent TGF-beta binding proteins: extracellular matrix association and roles in TGF-beta activation. Critical Reviews in Clinical Laboratory Sciences 41, 233264.CrossRefGoogle ScholarPubMed
Khalil, N et al. (2001) Regulation of the effects of TGF-beta 1 by activation of latent TGF-beta 1 and differential expression of TGF-beta receptors (T beta R-I and T beta R-II) in idiopathic pulmonary fibrosis. Thorax 56, 907915.CrossRefGoogle Scholar
Robertson, IB and Rifkin, DB (2016) Regulation of the bioavailability of TGF-beta and TGF-beta-related proteins. Cold Spring Harbor Perspectives in Biology 8, a021907.CrossRefGoogle ScholarPubMed
Wrana, JL et al. (1994) Mechanism of activation of the TGF-beta receptor. Nature 370, 341347.CrossRefGoogle ScholarPubMed
Rotzer, D et al. (2001) Type III TGF-beta receptor-independent signalling of TGF-beta2 via TbetaRII-B, an alternatively spliced TGF-beta type II receptor. EMBO Journal 20, 480490.CrossRefGoogle ScholarPubMed
Groppe, J et al. (2008) Cooperative assembly of TGF-beta superfamily signaling complexes is mediated by two disparate mechanisms and distinct modes of receptor binding. Molecular Cell 29, 157168.CrossRefGoogle ScholarPubMed
Zhang, Y et al. (1996) Receptor-associated Mad homologues synergize as effectors of the TGF-beta response. Nature 383, 168172.CrossRefGoogle ScholarPubMed
Piek, E et al. (1999) TGF-(beta) type I receptor/ALK-5 and Smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells. Journal of Cell Science 112, 45574568.CrossRefGoogle ScholarPubMed
Matsuzaki, K (2012) Smad phosphoisoform signals in acute and chronic liver injury: similarities and differences between epithelial and mesenchymal cells. Cell and Tissue Research 347, 225243.CrossRefGoogle ScholarPubMed
Xiao, Z et al. (2001) Nucleocytoplasmic shuttling of Smad1 conferred by its nuclear localization and nuclear export signals. Journal of Biological Chemistry 276, 3940439410.CrossRefGoogle ScholarPubMed
Wang, G et al. (2005) The Smad3 linker region contains a transcriptional activation domain. Biochemical Journal 386(Pt ), 2934.CrossRefGoogle ScholarPubMed
Hanyu, A et al. (2001) The N domain of Smad7 is essential for specific inhibition of transforming growth factor-beta signaling. Journal of Cell Biology 155, 10171027.CrossRefGoogle Scholar
Yi, JY, Shin, I and Arteaga, CL (2005) Type I transforming growth factor beta receptor binds to and activates phosphatidylinositol 3-kinase. Journal of Biological Chemistry 280, 10870–6.CrossRefGoogle ScholarPubMed
Lamouille, S et al. (2012) TGF-beta-induced activation of mTOR complex 2 drives epithelial-mesenchymal transition and cell invasion. Journal of Cell Science 125, 12591273.CrossRefGoogle ScholarPubMed
Lee, MK et al. (2007) TGF-beta activates Erk MAP kinase signalling through direct phosphorylation of ShcA. EMBO Journal 26, 39573967.CrossRefGoogle ScholarPubMed
Yamashita, M et al. (2008) TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-beta. Molecular Cell 31, 918924.CrossRefGoogle ScholarPubMed
Lin, A et al. (1995) Identification of a dual specificity kinase that activates the Jun kinases and p38-Mpk2. Science 268, 286290.CrossRefGoogle ScholarPubMed
Zhang, L et al. (2013) TRAF4 promotes TGF-beta receptor signaling and drives breast cancer metastasis. Molecular Cell 51, 559572.CrossRefGoogle ScholarPubMed
Hamidi, A et al. (2012) Polyubiquitination of transforming growth factor beta (TGFbeta)-associated kinase 1 mediates nuclear factor-kappaB activation in response to different inflammatory stimuli. Journal of Biological Chemistry 287, 123133.CrossRefGoogle ScholarPubMed
Liu, C et al. (2009) TACE-mediated ectodomain shedding of the type I TGF-beta receptor downregulates TGF-beta signaling. Molecular Cell 35, 2636.CrossRefGoogle ScholarPubMed
Gudey, SK et al. (2014) TRAF6 stimulates the tumor-promoting effects of TGFbeta type I receptor through polyubiquitination and activation of presenilin 1. Science Signaling 7, ra2.CrossRefGoogle ScholarPubMed
Dees, C et al. (2012) JAK-2 as a novel mediator of the profibrotic effects of transforming growth factor beta in systemic sclerosis. Arthritis and Rheumatism 64, 30063015.CrossRefGoogle ScholarPubMed
Tang, LY et al. (2017) Transforming growth factor-beta (TGF-beta) directly activates the JAK1-STAT3 axis to induce hepatic fibrosis in coordination with the SMAD pathway. Journal of Biological Chemistry 292, 43024312.CrossRefGoogle ScholarPubMed
Hanahan, D and Weinberg, RA (2000) The hallmarks of cancer. Cell 100, 5770.CrossRefGoogle ScholarPubMed
Hanahan, D and Weinberg, RA (2011) Hallmarks of cancer: the next generation. Cell 144, 646674.CrossRefGoogle ScholarPubMed
Hanahan, D (2022) Hallmarks of cancer: new dimensions. Cancer Discovery 12, 3146.CrossRefGoogle ScholarPubMed
Nagaraj, NS and Datta, PK (2010) Targeting the transforming growth factor-beta signaling pathway in human cancer. Expert Opinion on Investigational Drugs 19, 7791.CrossRefGoogle ScholarPubMed
Zhang, Y, Alexander, PB and Wang, XF (2017) TGF-beta family signaling in the control of cell proliferation and survival. Cold Spring Harbor Perspectives in Biology 9, a022145.CrossRefGoogle ScholarPubMed
Chen, CR, Kang, Y and Massague, J (2001) Defective repression of c-Myc in breast cancer cells: a loss at the core of the transforming growth factor beta growth arrest program. Proceedings of the National Academy of Sciences of the United States of America 98, 992999.CrossRefGoogle Scholar
Seoane, J et al. (2001) TGFbeta influences Myc, Miz-1 and Smad to control the CDK inhibitor p15INK4b. Nature Cell Biology 3, 400408.CrossRefGoogle ScholarPubMed
Seoane, J, Le, HV and Massague, J (2002) Myc suppression of the p21(Cip1) CDK inhibitor influences the outcome of the p53 response to DNA damage. Nature 419, 729734.CrossRefGoogle ScholarPubMed
Je, YJ et al. (2014) Inhibitory role of Id1 on TGF-beta-induced collagen expression in human dermal fibroblasts. Biochemical and Biophysical Research Communications 444, 8185.CrossRefGoogle ScholarPubMed
Selesniemi, K, Albers, RE and Brown, TL (2016) ID2 mediates differentiation of labyrinthine placental progenitor cell line, SM10. Stem Cells and Development 25, 959974.CrossRefGoogle ScholarPubMed
Karimian, A, Ahmadi, Y and Yousefi, B (2016) Multiple functions of p21 in cell cycle, apoptosis and transcriptional regulation after DNA damage. DNA Repair 42, 6371.CrossRefGoogle ScholarPubMed
Abbastabar, M et al. (2018) Multiple functions of p27 in cell cycle, apoptosis, epigenetic modification and transcriptional regulation for the control of cell growth: a double-edged sword protein. DNA Repair 69, 6372.CrossRefGoogle ScholarPubMed
Zhang, G et al. (2019) Long noncoding RNA ARHGAP27P1 inhibits gastric cancer cell proliferation and cell cycle progression through epigenetically regulating p15 and p16. Aging (Albany, NY) 11, 90909110.CrossRefGoogle ScholarPubMed
Chen, CR et al. (2002) E2F4/5 and p107 as Smad cofactors linking the TGFbeta receptor to c-Myc repression. Cell 110, 1932.CrossRefGoogle ScholarPubMed
Frederick, JP et al. (2004) Transforming growth factor beta-mediated transcriptional repression of c-Myc is dependent on direct binding of Smad3 to a novel repressive Smad binding element. Molecular and Cellular Biology 24, 25462559.CrossRefGoogle ScholarPubMed
Liu, FS et al. (2003) Loss of Smad4 protein expression occurs infrequently in endometrial carcinomas. International Journal of Gynecological Pathology 22, 347352.CrossRefGoogle ScholarPubMed
Papageorgis, P (2015) TGFbeta signaling in tumor initiation, epithelial-to-mesenchymal transition, and metastasis. Journal of Oncology 2015, 587193.CrossRefGoogle ScholarPubMed
Zhou, HH et al. (2016) Smad3 sensitizes hepatocelluar carcinoma cells to cisplatin by repressing phosphorylation of AKT. International Journal of Molecular Sciences 17, 610.CrossRefGoogle ScholarPubMed
Bakkebo, M et al. (2010) TGF-beta-induced growth inhibition in B-cell lymphoma correlates with Smad1/5 signalling and constitutively active p38 MAPK. BMC Immunology 11, 57.CrossRefGoogle ScholarPubMed
Yang, Y et al. (2021) The role of TGF-beta signaling pathways in cancer and Its potential as a therapeutic target. Evidence-Based Complementary and Alternative Medicine: ECAM 2021, 6675208.Google ScholarPubMed
Jang, CW et al. (2002) TGF-beta induces apoptosis through Smad-mediated expression of DAP-kinase. Nature Cell Biology 4, 5158.CrossRefGoogle ScholarPubMed
Valderrama-Carvajal, H et al. (2002) Activin/TGF-beta induce apoptosis through Smad-dependent expression of the lipid phosphatase SHIP. Nature Cell Biology 4, 963969.CrossRefGoogle ScholarPubMed
Chalaux, E et al. (1999) A zinc-finger transcription factor induced by TGF-beta promotes apoptotic cell death in epithelial Mv1Lu cells. FEBS Letters 457, 478482.CrossRefGoogle ScholarPubMed
Kammoun, M et al. (2020) Novel role of Tieg1 in muscle metabolism and mitochondrial oxidative capacities. Acta Physiologica 228, e13394.CrossRefGoogle ScholarPubMed
Francis, JM et al. (2000) Transforming growth factor-beta 1 induces apoptosis independently of p53 and selectively reduces expression of Bcl-2 in multipotent hematopoietic cells. Journal of Biological Chemistry 275, 3913739145.CrossRefGoogle ScholarPubMed
Huang, EJ et al. (2006) Opposing action of estrogen receptors alpha and beta on tumor necrosis factor-alpha gene expression and caspase-8-mediated apoptotic effects in HA22T cells. Molecular and Cellular Biochemistry 287, 137145.CrossRefGoogle ScholarPubMed
Ramjaun, AR et al. (2007) Upregulation of two BH3-only proteins, BMF and BIM, during TGF beta-induced apoptosis. Oncogene 26, 970981.CrossRefGoogle ScholarPubMed
David, CJ et al. (2016) TGF-beta tumor suppression through a lethal EMT. Cell 164, 10151030.CrossRefGoogle ScholarPubMed
Ehata, S et al. (2007) Transforming growth factor-beta promotes survival of mammary carcinoma cells through induction of antiapoptotic transcription factor DEC1. Cancer Research 67, 96949703.CrossRefGoogle ScholarPubMed
Schlapbach, R et al. (2000) TGF-beta induces the expression of the FLICE-inhibitory protein and inhibits Fas-mediated apoptosis of microglia. European Journal of Immunology 30, 36803688.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Wu, X, Won, H and Rubinsztein, DC (2013) Autophagy and mammalian development. Biochemical Society Transactions 41, 14891494.CrossRefGoogle ScholarPubMed
Kiyono, K et al. (2009) Autophagy is activated by TGF-beta and potentiates TGF-beta-mediated growth inhibition in human hepatocellular carcinoma cells. Cancer Research 69, 88448852.CrossRefGoogle ScholarPubMed
Suzuki, HI, Kiyono, K and Miyazono, K (2010) Regulation of autophagy by transforming growth factor-beta (TGF-beta) signaling. Autophagy 6, 645647.CrossRefGoogle ScholarPubMed
Chen, X et al. (2021) Broadening horizons: the role of ferroptosis in cancer. Nature Reviews. Clinical Oncology 18, 280296.CrossRefGoogle ScholarPubMed
Kim, DH et al. (2020) TGF-beta1-mediated repression of SLC7A11 drives vulnerability to GPX4 inhibition in hepatocellular carcinoma cells. Cell Death & Disease 11, 406.CrossRefGoogle ScholarPubMed
Jorgensen, I and Miao, EA (2015) Pyroptotic cell death defends against intracellular pathogens. Immunological Reviews 265, 130142.CrossRefGoogle ScholarPubMed
Xia, X et al. (2019) The role of pyroptosis in cancer: pro-cancer or pro-‘host’? Cell Death & Disease 10, 650.CrossRefGoogle ScholarPubMed
Jiang, R et al. (2020) MiR-21-5p induces pyroptosis in colorectal cancer via TGFBI. Frontiers in Oncology 10, 610545.CrossRefGoogle ScholarPubMed
Tamura, Y et al. (2021) Anti-pyroptotic function of TGF-beta is suppressed by a synthetic dsRNA analogue in triple negative breast cancer cells. Molecular Oncology 15, 12891307.CrossRefGoogle ScholarPubMed
Elston, R and Inman, GJ (2012) Crosstalk between p53 and TGF-beta signalling. Journal of Signal Transduction, 2012, 294097.CrossRefGoogle ScholarPubMed
Cordenonsi, M et al. (2003) Links between tumor suppressors: p53 is required for TGF-beta gene responses by cooperating with Smads. Cell 113, 301314.CrossRefGoogle ScholarPubMed
Dupont, S et al. (2004) Convergence of p53 and TGF-beta signaling networks. Cancer Letters 213, 129138.CrossRefGoogle ScholarPubMed
Cordenonsi, M et al. (2007) Integration of TGF-beta and Ras/MAPK signaling through p53 phosphorylation. Science 315, 840843.CrossRefGoogle ScholarPubMed
Atfi, A and Baron, R (2008) P53 brings a new twist to the Smad signaling network. Science Signaling 1, pe33.CrossRefGoogle Scholar
Adorno, M et al. (2009) A mutant-p53/Smad complex opposes p63 to empower TGFbeta-induced metastasis. Cell 137, 8798.CrossRefGoogle ScholarPubMed
Kalo, E et al. (2007) Mutant p53 attenuates the SMAD-dependent transforming growth factor beta1 (TGF-beta1) signaling pathway by repressing the expression of TGF-beta receptor type II. Molecular and Cellular Biology 27, 82288242.CrossRefGoogle ScholarPubMed
Carmeliet, P and Jain, RK (2000) Angiogenesis in cancer and other diseases. Nature 407, 249257.CrossRefGoogle ScholarPubMed
Roberts, AB et al. (1988) Transforming growth factor-beta: possible roles in carcinogenesis. British Journal of Cancer 57, 594600.CrossRefGoogle ScholarPubMed
Tian, M and Schiemann, WP (2009) The TGF-beta paradox in human cancer: an update. Future Oncology 5, 259271.CrossRefGoogle ScholarPubMed
Shimo, T et al. (2001) Involvement of CTGF, a hypertrophic chondrocyte-specific gene product, in tumor angiogenesis. Oncology 61, 315322.CrossRefGoogle ScholarPubMed
Fang, L et al. (2020) TGF-beta1 induces VEGF expression in human granulosa-lutein cells: a potential mechanism for the pathogenesis of ovarian hyperstimulation syndrome. Experimental and Molecular Medicine 52, 450460.CrossRefGoogle ScholarPubMed
Rak, J et al. (2000) Oncogenes and tumor angiogenesis: differential modes of vascular endothelial growth factor up-regulation in RAS-transformed epithelial cells and fibroblasts. Cancer Research 60, 490498.Google ScholarPubMed
Groppa, E et al. (2015) VEGF dose regulates vascular stabilization through semaphorin3A and the neuropilin-1 + monocyte/TGF-beta1 paracrine axis. EMBO Molecular Medicine 7, 13661384.CrossRefGoogle ScholarPubMed
Wang, J et al. (2013) Transforming growth factor beta-regulated microRNA-29a promotes angiogenesis through targeting the phosphatase and tensin homolog in endothelium. Journal of Biological Chemistry 288, 1041810426.CrossRefGoogle ScholarPubMed
Miyazono, K, Ehata, S and Koinuma, D (2012) Tumor-promoting functions of transforming growth factor-beta in progression of cancer. Upsala Journal of Medical Sciences 117, 143152.CrossRefGoogle ScholarPubMed
Zonneville, J et al. (2018) TGF-beta signaling promotes tumor vasculature by enhancing the pericyte-endothelium association. BMC Cancer 18, 670.CrossRefGoogle ScholarPubMed
Hoshino, A et al. (2015) Tumour exosome integrins determine organotropic metastasis. Nature 527, 329335.CrossRefGoogle ScholarPubMed
Lambert, AW, Pattabiraman, DR and Weinberg, RA (2017) Emerging biological principles of metastasis. Cell 168, 670691.CrossRefGoogle ScholarPubMed
Chiang, AC and Massague, J (2008) Molecular basis of metastasis. New England Journal of Medicine 359, 28142823.CrossRefGoogle ScholarPubMed
Tsai, JH and Yang, J (2013) Epithelial-mesenchymal plasticity in carcinoma metastasis. Genes & Development 27, 21922206.CrossRefGoogle ScholarPubMed
Lamouille, S, Xu, J and Derynck, R (2014) Molecular mechanisms of epithelial-mesenchymal transition. Nature Reviews Molecular Cell Biology 15, 178196.CrossRefGoogle ScholarPubMed
Deckers, M et al. (2006) The tumor suppressor Smad4 is required for transforming growth factor beta-induced epithelial to mesenchymal transition and bone metastasis of breast cancer cells. Cancer Research 66, 22022209.CrossRefGoogle ScholarPubMed
Ju, W et al. (2006) Deletion of Smad2 in mouse liver reveals novel functions in hepatocyte growth and differentiation. Molecular and Cellular Biology 26, 654667.CrossRefGoogle ScholarPubMed
Neuzillet, C et al. (2015) Targeting the TGFbeta pathway for cancer therapy. Pharmacology & Therapeutics 147, 2231.CrossRefGoogle ScholarPubMed
Principe, DR et al. (2014) TGF-beta: duality of function between tumor prevention and carcinogenesis. Journal of the National Cancer Institute 106, djt369.CrossRefGoogle ScholarPubMed
Liu, J et al. (2020) Circ-OXCT1 suppresses gastric cancer EMT and metastasis by attenuating TGF-beta pathway through the circ-OXCT1/miR-136/SMAD4 axis. OncoTargets and Therapy 13, 39873998.CrossRefGoogle ScholarPubMed
Tang, L et al. (2020) DCST1-AS1 promotes TGF-beta-induced epithelial-mesenchymal transition and enhances chemoresistance in triple-negative breast cancer cells via ANXA1. Frontiers in Oncology 10, 280.CrossRefGoogle ScholarPubMed
Wang, Z et al. (2020) HCK promotes glioblastoma progression by TGFbeta signaling. Bioscience Reports 40, BSR20200975.CrossRefGoogle ScholarPubMed
Landstrom, M (2010) The TAK1-TRAF6 signalling pathway. International Journal of Biochemistry & Cell Biology 42, 585589.CrossRefGoogle ScholarPubMed
Song, J and Landstrom, M (2017) TGFbeta activates PI3K-AKT signaling via TRAF6. Oncotarget 8, 9920599206.CrossRefGoogle ScholarPubMed
Lin, T et al. (2003) Rho-ROCK-LIMK-cofilin pathway regulates shear stress activation of sterol regulatory element binding proteins. Circulation Research 92, 12961304.CrossRefGoogle ScholarPubMed
Lindsey, S and Langhans, SA (2014) Crosstalk of oncogenic signaling pathways during epithelial–mesenchymal transition. Frontiers in Oncology 4, 358.CrossRefGoogle ScholarPubMed
Lee, EK et al. (2010) Decreased expression of glutaredoxin 1 is required for transforming growth factor-beta1-mediated epithelial-mesenchymal transition of EpRas mammary epithelial cells. Biochemical and Biophysical Research Communications 391, 10211027.CrossRefGoogle ScholarPubMed
Peng, X et al. (2018) SOX4 contributes to TGF-beta-induced epithelial-mesenchymal transition and stem cell characteristics of gastric cancer cells. Genes & Diseases 5, 4961.CrossRefGoogle ScholarPubMed
Nong, S et al. (2022) HN1L promotes stem cell-like properties by regulating TGF-beta signaling pathway through targeting FOXP2 in prostate cancer. Cell Biology International 46, 8395.CrossRefGoogle ScholarPubMed
Zhang, B et al. (2019) Macrophage-expressed CD51 promotes cancer stem cell properties via the TGF-beta1/smad2/3 axis in pancreatic cancer. Cancer Letters 459, 204215.CrossRefGoogle ScholarPubMed
Wang, L et al. (2021) Up-regulation of miR-663a inhibits the cancer stem cell-like properties of glioma via repressing the KDM2A-mediated TGF-beta/SMAD signaling pathway. Cell Cycle 20, 19351952.CrossRefGoogle ScholarPubMed
Chen, J and Gingold, AJ (2020) Dysregulated PJA1-TGF-beta signaling in cancer stem cell-associated liver cancers. Oncoscience 7, 8895.CrossRefGoogle ScholarPubMed
Candido, J and Hagemann, T (2013) Cancer-related inflammation. Journal of Clinical Immunology 33 (Suppl. 1), S79S84.CrossRefGoogle ScholarPubMed
Landskron, G et al. (2014) Chronic inflammation and cytokines in the tumor microenvironment. Journal of Immunology Research 2014, 149185.CrossRefGoogle ScholarPubMed
Chen, W and Ten Dijke, P (2016) Immunoregulation by members of the TGFbeta superfamily. Nature Reviews Immunology 16, 723740.CrossRefGoogle ScholarPubMed
Sanjabi, S, Oh, SA and Li, MO (2017) Regulation of the immune response by TGF-beta: from conception to autoimmunity and infection. Cold Spring Harbor Perspectives in Biology 9, a022236.CrossRefGoogle ScholarPubMed
Fu, S et al. (2004) TGF-beta induces Foxp3+ T-regulatory cells from CD4+ CD25-precursors. American Journal of Transplantation 4, 16141627.CrossRefGoogle ScholarPubMed
Ludviksson, BR et al. (2000) The effect of TGF-beta1 on immune responses of naive versus memory CD4+ Th1/Th2 T cells. European Journal of Immunology 30, 21012111.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
Mangan, PR et al. (2006) Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441, 231234.CrossRefGoogle Scholar
Papaspyridonos, M et al. (2015) ID1 suppresses anti-tumour immune responses and promotes tumour progression by impairing myeloid cell maturation. Nature Communications 6, 6840.CrossRefGoogle ScholarPubMed
Song, S et al. (2014) Dendritic cells with an increased PD-L1 by TGF-beta induce T cell anergy for the cytotoxicity of hepatocellular carcinoma cells. International Immunopharmacology 20, 117123.CrossRefGoogle ScholarPubMed
Eriksson, E et al. (2019) IL-6 signaling blockade during CD40-mediated immune activation favors antitumor factors by reducing TGF-beta, collagen type I, and PD-L1/PD-1. Journal of Immunology 202, 787798.CrossRefGoogle ScholarPubMed
Friese, MA et al. (2004) RNA interference targeting transforming growth factor-beta enhances NKG2D-mediated antiglioma immune response, inhibits glioma cell migration and invasiveness, and abrogates tumorigenicity in vivo. Cancer Research 64, 75967603.CrossRefGoogle ScholarPubMed
Lazarova, M and Steinle, A (2019) Impairment of NKG2D-mediated tumor immunity by TGF-beta. Frontiers in Immunology 10, 2689.CrossRefGoogle ScholarPubMed
Gong, D et al. (2012) TGFbeta signaling plays a critical role in promoting alternative macrophage activation. BMC Immunology 13, 31.CrossRefGoogle Scholar
Fridlender, ZG et al. (2009) Polarization of tumor-associated neutrophil phenotype by TGF-beta: ‘N1’ versus ‘N2’ TAN. Cancer Cell 16, 183194.CrossRefGoogle ScholarPubMed
Gallego-Valle, J et al. (2021) Ectopic FOXP3 expression in combination with TGF-beta1 and IL-2 stimulation generates limited suppressive function in human primary activated thymocytes ex vivo. Biomedicines 9, 461.CrossRefGoogle ScholarPubMed
Diamond, MS et al. (2011) Type I interferon is selectively required by dendritic cells for immune rejection of tumors. Journal of Experimental Medicine 208, 19892003.CrossRefGoogle ScholarPubMed
Caligiuri, MA (2008) Human natural killer cells. Blood 112, 461469.CrossRefGoogle ScholarPubMed
Siegert, A et al. (1999) Suppression of the reactive oxygen intermediates production of human macrophages by colorectal adenocarcinoma cell lines. Immunology 98, 551556.CrossRefGoogle ScholarPubMed
Wu, J and Lanier, LL (2003) Natural killer cells and cancer. Advances in Cancer Research 90, 127156.CrossRefGoogle ScholarPubMed
Grosser, R et al. (2019) Combination immunotherapy with CAR T cells and checkpoint blockade for the treatment of solid tumors. Cancer Cell 36, 471482.CrossRefGoogle Scholar
Gorelik, L and Flavell, RA (2000) Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 12, 171181.CrossRefGoogle Scholar
Gatenby, RA and Gillies, RJ (2004) Why do cancers have high aerobic glycolysis? Nature Reviews Cancer 4, 891899.CrossRefGoogle ScholarPubMed
Zadran, S et al. (2014) Surprisal analysis characterizes the free energy time course of cancer cells undergoing epithelial-to-mesenchymal transition. Proceedings of the National Academy of Sciences of the USA 111, 1323513240.CrossRefGoogle ScholarPubMed
Santos, CR and Schulze, A (2012) Lipid metabolism in cancer. FEBS Journal 279, 26102623.CrossRefGoogle ScholarPubMed
Luo, X et al. (2017) Emerging roles of lipid metabolism in cancer metastasis. Molecular Cancer 16, 76.CrossRefGoogle ScholarPubMed
Altenberg, B and Greulich, KO (2004) Genes of glycolysis are ubiquitously overexpressed in 24 cancer classes. Genomics 84, 10141020.CrossRefGoogle ScholarPubMed
Li, W et al. (2010) Increased 18F-FDG uptake and expression of Glut1 in the EMT transformed breast cancer cells induced by TGF-beta. Neoplasma 57, 234240.CrossRefGoogle ScholarPubMed
De Bock, K et al. (2013) Role of PFKFB3-driven glycolysis in vessel sprouting. Cell 154, 651663.CrossRefGoogle ScholarPubMed
Rodriguez-Garcia, A et al. (2017) TGF-beta1 targets Smad, p38 MAPK, and PI3K/Akt signaling pathways to induce PFKFB3 gene expression and glycolysis in glioblastoma cells. FEBS Journal 284, 34373454.CrossRefGoogle ScholarPubMed
Guerra, F et al. (2017) Mitochondrial dysfunction: a novel potential driver of epithelial-to-mesenchymal transition in cancer. Frontiers in Oncology 7, 295.CrossRefGoogle ScholarPubMed
Martinez-Outschoorn, UE, Sotgia, F and Lisanti, MP (2012) Power surge: supporting cells ‘fuel’ cancer cell mitochondria. Cell Metabolism 15, 45.CrossRefGoogle ScholarPubMed
Beloribi-Djefaflia, S, Vasseur, S and Guillaumond, F (2016) Lipid metabolic reprogramming in cancer cells. Oncogenesis 5, e189.CrossRefGoogle ScholarPubMed
Menendez, JA and Lupu, R (2017) Fatty acid synthase (FASN) as a therapeutic target in breast cancer. Expert Opinion on Therapeutic Targets 21, 10011016.CrossRefGoogle ScholarPubMed
Angioni, R et al. (2021) TGF-beta in cancer: metabolic driver of the tolerogenic crosstalk in the tumor microenvironment. Cancers (Basel) 13, 401.CrossRefGoogle ScholarPubMed
Dimeloe, S et al. (2019) Tumor-derived TGF-beta inhibits mitochondrial respiration to suppress IFN-gamma production by human CD4(+) T cells. Science Signaling 12(599), eaav3334.CrossRefGoogle ScholarPubMed
Priyadharshini, B et al. (2018) Cutting edge: TGF-beta and phosphatidylinositol 3-kinase signals modulate distinct metabolism of regulatory T cell subsets. Journal of Immunology 201, 22152219.CrossRefGoogle ScholarPubMed
Coppe, JP et al. (2010) The senescence-associated secretory phenotype: the dark side of tumor suppression. Annual Review of Pathology 5, 99118.CrossRefGoogle ScholarPubMed
Ding, MJ et al. (2016) Association between transforming growth factor-beta1 expression and the clinical features of triple negative breast cancer. Oncology Letters 11, 40404044.CrossRefGoogle ScholarPubMed
Roy, LO, Poirier, MB and Fortin, D (2018) Differential expression and clinical significance of transforming growth factor-beta isoforms in GBM tumors. International Journal of Molecular Sciences 19, 1113.CrossRefGoogle ScholarPubMed
Akhurst, RJ (2017) Targeting TGF-beta signaling for therapeutic gain. Cold Spring Harbor Perspectives in Biology 9, a022301.CrossRefGoogle ScholarPubMed
Kim, BG et al. (2021) Novel therapies emerging in oncology to target the TGF-beta pathway. Journal of Hematology & Oncology 14, 55.CrossRefGoogle ScholarPubMed
Huynh, LK, Hipolito, CJ and Ten Dijke, P (2019) A perspective on the development of TGF-beta inhibitors for cancer treatment. Biomolecules 9, 743.CrossRefGoogle ScholarPubMed
Jin, CH et al. (2014) Discovery of N-((4-([1,2,4]triazolo [1,5-a]pyridin-6-yl)-5-(6-methylpyridin-2-yl)-1H-imidazol-2-yl)methyl)-2-fluoroaniline (EW-7197): a highly potent, selective, and orally bioavailable inhibitor of TGF-beta type I receptor kinase as cancer immunotherapeutic/antifibrotic agent. Journal of Medicinal Chemistry 57, 42134238.CrossRefGoogle Scholar
Fujiwara, Y et al. (2015) Phase 1 study of galunisertib, a TGF-beta receptor I kinase inhibitor, in Japanese patients with advanced solid tumors. Cancer Chemotherapy and Pharmacology 76, 11431152.CrossRefGoogle ScholarPubMed
Yap, TA et al. (2021) First-in-human phase I study of a next-generation, oral, TGFbeta receptor 1 inhibitor, LY3200882, in patients with advanced cancer. Clinical Cancer Research 27, 66666676.CrossRefGoogle ScholarPubMed
Inman, GJ et al. (2002) SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Molecular Pharmacology 62, 6574.CrossRefGoogle ScholarPubMed
Yingling, JM et al. (2018) Preclinical assessment of galunisertib (LY2157299 monohydrate), a first-in-class transforming growth factor-beta receptor type I inhibitor. Oncotarget 9, 66596677.CrossRefGoogle ScholarPubMed
Yang, YA et al. (2002) Lifetime exposure to a soluble TGF-beta antagonist protects mice against metastasis without adverse side effects. Journal of Clinical Investigation 109, 16071615.CrossRefGoogle ScholarPubMed
Hinck, AP and O'Connor-McCourt, MD (2011) Structures of TGF-beta receptor complexes: implications for function and therapeutic intervention using ligand traps. Current Pharmaceutical Biotechnology 12, 20812098.CrossRefGoogle ScholarPubMed
Lan, Y et al. (2018) Enhanced preclinical antitumor activity of M7824, a bifunctional fusion protein simultaneously targeting PD-L1 and TGF-beta. Science Translational Medicine 10, eaan5488.CrossRefGoogle ScholarPubMed
Zwaagstra, JC et al. (2012) Engineering and therapeutic application of single-chain bivalent TGF-beta family traps. Molecular Cancer Therapeutics 11, 14771487.CrossRefGoogle ScholarPubMed
Qin, T et al. (2016) A novel highly potent trivalent TGF-beta receptor trap inhibits early-stage tumorigenesis and tumor cell invasion in murine Pten-deficient prostate glands. Oncotarget 7, 8608786102.CrossRefGoogle ScholarPubMed
Tremblay, D and Mascarenhas, J (2021) Next generation therapeutics for the treatment of myelofibrosis. Cells 10, 1034.CrossRefGoogle ScholarPubMed
Strauss, J et al. (2018) Phase I trial of M7824 (MSB0011359C), a bifunctional fusion protein targeting PD-L1 and TGFbeta, in advanced solid tumors. Clinical Cancer Research 24, 12871295.CrossRefGoogle ScholarPubMed
Fenaux, P et al. (2020) Luspatercept in patients with lower-risk myelodysplastic syndromes. New England Journal of Medicine 382, 140151.CrossRefGoogle ScholarPubMed
Morris, JC et al. (2014) Phase I study of GC1008 (fresolimumab): a human anti-transforming growth factor-beta (TGFbeta) monoclonal antibody in patients with advanced malignant melanoma or renal cell carcinoma. PLoS ONE 9, e90353.CrossRefGoogle ScholarPubMed
Eberlein, C et al. (2013) A human monoclonal antibody 264RAD targeting alphavbeta6 integrin reduces tumour growth and metastasis, and modulates key biomarkers in vivo. Oncogene 32, 44064416.CrossRefGoogle ScholarPubMed
Nam, JS et al. (2008) An anti-transforming growth factor beta antibody suppresses metastasis via cooperative effects on multiple cell compartments. Cancer Research 68, 38353843.CrossRefGoogle ScholarPubMed
Bedinger, D et al. (2016) Development and characterization of human monoclonal antibodies that neutralize multiple TGFbeta isoforms. MAbs 8, 389404.CrossRefGoogle ScholarPubMed
Greco, R et al. (2020) Pan-TGFbeta inhibition by SAR439459 relieves immunosuppression and improves antitumor efficacy of PD-1 blockade. Oncoimmunology 9, 1811605.CrossRefGoogle ScholarPubMed
Gleave, ME and Monia, BP (2005) Antisense therapy for cancer. Nature Reviews Cancer 5, 468479.CrossRefGoogle ScholarPubMed
Dias, N and Stein, CA (2002) Antisense oligonucleotides: basic concepts and mechanisms. Molecular Cancer Therapeutics 1, 347355.Google ScholarPubMed
Tibbitt, MW, Dahlman, JE and Langer, R (2016) Emerging frontiers in drug delivery. Journal of the American Chemical Society 138, 704717.CrossRefGoogle ScholarPubMed
Hau, P et al. (2007) Inhibition of TGF-beta2 with AP 12009 in recurrent malignant gliomas: from preclinical to phase I/II studies. Oligonucleotides 17, 201212.CrossRefGoogle ScholarPubMed
Huber-Ruano, I et al. (2017) An antisense oligonucleotide targeting TGF-beta2 inhibits lung metastasis and induces CD86 expression in tumor-associated macrophages. Annals of Oncology 28, 22782285.CrossRefGoogle ScholarPubMed
Massague, J (2008) TGFbeta in cancer. Cell 134, 215230.CrossRefGoogle ScholarPubMed
Colak, S and Ten Dijke, P (2017) Targeting TGF-beta signaling in cancer. Trends in Cancer 3, 5671.CrossRefGoogle ScholarPubMed
Arteaga, CL et al. (1993) Anti-transforming growth factor (TGF)-beta antibodies inhibit breast cancer cell tumorigenicity and increase mouse spleen natural killer cell activity. Implications for a possible role of tumor cell/host TGF-beta interactions in human breast cancer progression. Journal of Clinical Investigation 92, 25692576.CrossRefGoogle ScholarPubMed
Mariathasan, S et al. (2018) TGFbeta attenuates tumour response to PD-L1 blockade by contributing to exclusion of T cells. Nature 554, 544548.CrossRefGoogle ScholarPubMed
Tauriello, DVF et al. (2018) TGFbeta drives immune evasion in genetically reconstituted colon cancer metastasis. Nature 554, 538543.CrossRefGoogle ScholarPubMed
Martin, CJ et al. (2020) Selective inhibition of TGFbeta1 activation overcomes primary resistance to checkpoint blockade therapy by altering tumor immune landscape. Science Translational Medicine 12, eaay8456.CrossRefGoogle ScholarPubMed
Groeneveldt, C et al. (2020) Immunotherapeutic potential of TGF-beta inhibition and oncolytic viruses. Trends in Immunology 41, 406420.CrossRefGoogle ScholarPubMed
Hutzen, B et al. (2017) TGF-beta Inhibition improves oncolytic herpes viroimmunotherapy in murine models of rhabdomyosarcoma. Molecular Therapy Oncolytics 7, 1726.CrossRefGoogle ScholarPubMed
Esaki, S et al. (2017) Blockade of transforming growth factor-beta signaling enhances oncolytic herpes simplex virus efficacy in patient-derived recurrent glioblastoma models. International Journal of Cancer 141, 23482358.CrossRefGoogle ScholarPubMed
Han, J et al. (2015) TGFbeta treatment enhances glioblastoma virotherapy by inhibiting the innate immune response. Cancer Research 75, 52735282.CrossRefGoogle ScholarPubMed
Seth, P et al. (2006) Development of oncolytic adenovirus armed with a fusion of soluble transforming growth factor-beta receptor II and human immunoglobulin Fc for breast cancer therapy. Human Gene Therapy 17, 11521160.CrossRefGoogle ScholarPubMed
Hu, Z et al. (2012) Systemic delivery of oncolytic adenoviruses targeting transforming growth factor-beta inhibits established bone metastasis in a prostate cancer mouse model. Human Gene Therapy 23, 871882.CrossRefGoogle Scholar
Larson, C et al. (2021) Toxicology and biodistribution of AdAPT-001, a replication-competent type 5 adenovirus with a trap for the immunosuppressive cytokine, TGF-beta. American Journal of Cancer Research 11, 51845189.Google ScholarPubMed
Zhang, M et al. (2021) TGF-beta signaling and resistance to cancer therapy. Frontiers in Cell and Developmental Biology 9, 786728.CrossRefGoogle ScholarPubMed
Ewan, KB et al. (2002) Transforming growth factor-beta1 mediates cellular response to DNA damage in situ. Cancer Research 62, 56275631.Google ScholarPubMed
Wang, J et al. (2021) TGF-beta signaling in cancer radiotherapy. Cytokine 148, 155709.CrossRefGoogle ScholarPubMed
Formenti, SC et al. (2018) Focal irradiation and systemic TGFbeta blockade in metastatic breast cancer. Clinical Cancer Research 24, 24932504.CrossRefGoogle ScholarPubMed
Dai, X et al. (2018) The emerging role of gas plasma in oncotherapy. Trends in Biotechnology 36, 11831198.CrossRefGoogle ScholarPubMed
Breathnach, R et al. (2018) Evaluation of the effectiveness of kINPen Med plasma jet and bioactive agent therapy in a rat model of wound healing. Biointerphases 13, 051002.CrossRefGoogle Scholar
Maisch, T et al. (2017) Investigation of toxicity and mutagenicity of cold atmospheric argon plasma. Environmental and Molecular Mutagenesis 58, 172177.CrossRefGoogle ScholarPubMed
Brehmer, F et al. (2015) Alleviation of chronic venous leg ulcers with a hand-held dielectric barrier discharge plasma generator (PlasmaDerm1 VU-2010): results of a monocentric, two-armed, open, prospective, randomized and controlled trial (NCT01415622). The Journal of the European Academy of Dermatology and Venereology 29, 148155.CrossRefGoogle ScholarPubMed
Gjika, E et al. (2017) The cutting mechanism of the electrosurgical scalpel. Journal of Physics D: Applied Physics 50, 025401.CrossRefGoogle Scholar
Xiang, L et al. (2018) Cold atmospheric plasma conveys selectivity on triple negative breast cancer cells both in vitro and in vivo. Free Radical Biology & Medicine 124, 205213.CrossRefGoogle ScholarPubMed
Zhou, X et al. (2020) InvivoPen: a novel plasma source for in vivo cancer treatment. Journal of Cancer 11, 22732282.CrossRefGoogle ScholarPubMed
Hua, D et al. (2021) Cold atmospheric plasma selectively induces G0/G1 cell cycle arrest and apoptosis in AR-independent prostate cancer cells. Journal of Cancer 12, 59775986.CrossRefGoogle ScholarPubMed
Wang, P et al. (2021) Epithelial-to-mesenchymal transition enhances cancer cell sensitivity to cytotoxic effects of cold atmospheric plasmas in breast and bladder cancer systems. Cancers (Basel) 13(12), 2889.CrossRefGoogle ScholarPubMed
Schneider, C et al. (2018) Cold atmospheric plasma causes a calcium influx in melanoma cells triggering CAP-induced senescence. Scientific Reports 8, 10048.CrossRefGoogle ScholarPubMed
Lin, A et al. (2019) Non-thermal plasma as a unique delivery system of short-lived reactive oxygen and nitrogen species for immunogenic cell death in melanoma cells. Advanced Science 6, 1802062.CrossRefGoogle ScholarPubMed
Miao, Y et al. (2021) Cold atmospheric plasma increases IBRV titer in MDBK cells by orchestrating the host cell network. Virulence 12, 679689.CrossRefGoogle ScholarPubMed
Virard, F et al. (2015) Cold atmospheric plasma induces a predominantly necrotic cell death via the microenvironment. PLoS ONE 10, e0133120.CrossRefGoogle ScholarPubMed
Furuta, T, Shi, L and Toyokuni, S (2018) Non-thermal plasma as a simple ferroptosis inducer in cancer cells: a possible role of ferritin. Pathology International 68, 442443.CrossRefGoogle ScholarPubMed
Bekeschus, S et al. (2020) xCT (SLC7A11) expression confers intrinsic resistance to physical plasma treatment in tumor cells. Redox Biology 30, 101423.CrossRefGoogle ScholarPubMed
Dai, X et al. (2019) Dosing: the key to precision plasma oncology. Plasma Processes and Polymers 17, e1900178.CrossRefGoogle Scholar
Yan, D et al. (2015) Toward understanding the selective anticancer capacity of cold atmospheric plasma--a model based on aquaporins. Biointerphases 10, 040801.CrossRefGoogle ScholarPubMed
Bauer, G et al. (2019) Dynamics of singlet oxygen-triggered, RONS-based apoptosis induction after treatment of tumor cells with cold atmospheric plasma or plasma-activated medium. Scientific Reports 9, 1393.Google ScholarPubMed
Dai, X et al. (2022) Cold atmospheric plasmas target breast cancer stemness via modulating AQP3-19Y mediated AQP3-5K and FOXO1 K48-ubiquitination. International Journal of Biological Sciences 18(8), 35443561.CrossRefGoogle ScholarPubMed
Dai, X et al. (2019) Key indexes and the emerging tool for tumor microenvironment editing. American Journal of Cancer Research 9, 10271042.Google ScholarPubMed
Park, S et al. (2019) Cold atmospheric plasma restores paclitaxel sensitivity to paclitaxel-resistant breast cancer cells by reversing expression of resistance-related genes. Cancers (Basel) 11, 2011.CrossRefGoogle ScholarPubMed
Miyamoto, K et al. (2016) Red blood cell coagulation induced by low-temperature plasma treatment. Archives of Biochemistry and Biophysics 605, 95101.CrossRefGoogle ScholarPubMed
Stratmann, B et al. (2020) Effect of cold atmospheric plasma therapy vs standard therapy placebo on wound healing in patients with diabetic foot ulcers: a randomized clinical trial. JAMA Netw Open 3, e2010411.CrossRefGoogle ScholarPubMed
Mark, P (2019) Plasma scalpel takes on cancer: a new tool enters a pivotal pilot study, in Scientific American. https://www.scientificamerican.com/article/plasma-scalpel-takes-on-cancer/.Google Scholar