Inhibitory effect of activin A on IL-9 production by mouse NK cells through Smad3 signaling

References

Ábrigo, J., Campos, F., Simon, F., Riedel, C., Cabrera, D., Vilos, C., and Cabello-Verrugio, C. (2018). TGF-β requires the activation of canonical and non-canonical signalling pathways to induce skeletal muscle atrophy. Biol. Chem. 399, 253–264.10.1515/hsz-2017-0217Search in Google Scholar PubMed

Bernard, D.J. and Tran, S. (2013). Mechanisms of activin-stimulated FSH synthesis: the story of a pig and a FOX. Biol. Reprod. 88, 78.10.1095/biolreprod.113.107797Search in Google Scholar PubMed

Bloise, E., Ciarmela, P., Dela Cruz, C., Luisi, S., Petraglia, F., and Reis, F.M. (2019). Activin A in mammalian physiology. Physiol. Rev. 99, 739–780.10.1152/physrev.00002.2018Search in Google Scholar PubMed

Chen, W. and Ten Dijke, P. (2016). Immunoregulation by members of the TGFβ superfamily. Nat. Rev. Immunol. 16, 723–740.10.1038/nri.2016.112Search in Google Scholar PubMed

Cui, X., Shang, S., Lv, X., Zhao, J., Qi, Y., and Liu, Z. (2019). Perspectives of small molecule inhibitors of activin receptor-like kinase in anti-tumor treatment and stem cell differentiation. Mol. Med. Rep. 19, 5053–5062.10.3892/mmr.2019.10209Search in Google Scholar PubMed PubMed Central

Elyaman, W., Bassil, R., Bradshaw, E.M., Orent, W., Lahoud, Y., Zhu, B., Radtke, F., Yagita, H., and Khoury, S.J. (2012). Notch receptors and Smad3 signaling cooperate in the induction of interleukin-9-producing T cells. Immunity 36, 623–634.10.1016/j.immuni.2012.01.020Search in Google Scholar PubMed PubMed Central

Fang, L., Wang, Y.N., Cui, X.L., Fang, S.Y., Ge, J.Y., Sun, Y., and Liu, Z.H. (2012). The role and mechanism of action of activin A in neurite outgrowth of chicken embryonic dorsal root ganglia. J. Cell. Sci. 125, 1500–1507.10.1242/jcs.094151Search in Google Scholar

Goswami, R. and Kaplan, M.H. (2011). A brief history of IL-9. J. Immunol. 186, 3283–3288.10.4049/jimmunol.1003049Search in Google Scholar PubMed PubMed Central

Handgretinger, R., Lang, P., and Andre, M.C. (2016). Exploitation of natural killer cells for the treatment of acute leukemia. Blood 127, 3341–3349.10.1182/blood-2015-12-629055Search in Google Scholar PubMed

Hultner, L., Kolsch, S., Stassen, M., Kaspers, U., Kremer, J.P., Mailhammer, R., Moeller, J., Broszeit, H., and Schmitt, E. (2000). In activated mast cells, IL-1 up-regulates the production of several Th2-related cytokines including IL-9. J. Immunol. 164, 5556–5563.10.4049/jimmunol.164.11.5556Search in Google Scholar PubMed

Li, N., Cui, X., Ge, J., Li, J., Niu, L., Liu, H., Qi, Y., Liu, Z., and Wang, Y. (2013). Activin A inhibits activities of lipopolysaccharide-activated macrophages via TLR4, not of TLR2. Biochem. Biophys. Res. Commun. 435, 222–228.10.1016/j.bbrc.2013.04.077Search in Google Scholar PubMed

Locci, M., Wu, J.E., Arumemi, F., Mikulski, Z., Dahlberg, C., Miller, A.T., and Crotty, S. (2016). Activin A programs the differentiation of human TFH cells. Nat. Immunol. 17, 976–984.10.1038/ni.3494Search in Google Scholar PubMed PubMed Central

Loomans, H.A. and Andl, C.D. (2014). Intertwining of activin A and TGFbeta signaling: dual roles in cancer progression and cancer cell invasion. Cancers (Basel) 7, 70–91.10.3390/cancers7010070Search in Google Scholar PubMed PubMed Central

Lu, A.Q., Popova, E.Y., and Barnstable, C.J. (2017). Activin signals through SMAD2/3 to increase photoreceptor precursor yield during embryonic stem cell differentiation. Stem Cell Rep. 9, 838–852.10.1016/j.stemcr.2017.06.021Search in Google Scholar PubMed PubMed Central

Luo, Z., Ji, Y., Tian, D., Zhang, Y., Chang, S., Yang, C., Zhou, H., and Chen, Z.K. (2018). Galectin-7 promotes proliferation and Th1/2 cells polarization toward Th1 in activated CD4+ T cells by inhibiting The TGFβ/Smad3 pathway. Mol. Immunol. 101, 80–85.10.1016/j.molimm.2018.06.003Search in Google Scholar PubMed

Ma, C., Liu, Z., Shang, S., Jiang, L., Lv, X., Qi, Y., Cui, X., and Ge, J. (2019). Activin A regulates activities of peripheral blood natural killer cells of mouse in an autocrine and paracrine manner. Exp. Cell Res. 374, 114–121.10.1016/j.yexcr.2018.11.013Search in Google Scholar PubMed

Matsuzawa, S., Sakashita, K., Kinoshita, T., Ito, S., Yamashita, T., and Koike, K. (2003). IL-9 enhances the growth of human mast cell progenitors under stimulation with stem cell factor. J. Immunol. 170, 3461–3467.10.4049/jimmunol.170.7.3461Search in Google Scholar PubMed

Meadows, S.K., Eriksson, M., Barber, A., and Sentman, C.L. (2006). Human NK cell IFN-gamma production is regulated by endogenous TGF-β. Int. Immunopharmacol. 6, 1020–1028.10.1016/j.intimp.2006.01.013Search in Google Scholar PubMed

Mesiano, G., Zini, R., Montagner, G., Bianchi, N., Manfredini, R., Chillemi, A., Aglietta, M., Grignani, G., Lampronti, I., Fiorino, E., et al. (2017). Analytic and dynamic secretory profile of patient-derived cytokine-induced killer cells. Mol. Med. 23, 235–246.10.2119/molmed.2017.00084Search in Google Scholar PubMed PubMed Central

Namwanje, M. and Brown, C.W. (2016). Activins and inhibins: roles in development, physiology, and disease. Cold Spring Harb. Perspect. Biol. 8, pii: a021881.10.1101/cshperspect.a021881Search in Google Scholar PubMed PubMed Central

Nowak, E.C., Weaver, C.T., Turner, H., Begum-Haque, S., Becher, B., Schreiner, B., Coyle, A.J., Kasper, L.H., and Noelle, R.J. (2009). IL-9 as a mediator of Th17-driven inflammatory disease. J. Exp. Med. 206, 1653–1660.10.1084/jem.20090246Search in Google Scholar PubMed PubMed Central

Ogawa, K., Funaba, M., Chen, Y., and Tsujimoto, M. (2006). Activin A functions as a Th2 cytokine in the promotion of the alternative activation of macrophages. J. Immunol. 177, 6787–6794.10.4049/jimmunol.177.10.6787Search in Google Scholar PubMed

Qi, Y., Ge, J., Ma, C., Wu, N., Cui, X., and Liu, Z. (2017). Activin A regulates activation of mouse neutrophils by Smad3 signalling. Open Biol. 7, pii: 160342.10.1098/rsob.160342Search in Google Scholar PubMed PubMed Central

Robson, N.C., Wei, H., McAlpine, T., Kirkpatrick, N., Cebon, J., and Maraskovsky, E. (2009). Activin-A attenuates several human natural killer cell functions. Blood 113, 3218–3225.10.1182/blood-2008-07-166926Search in Google Scholar PubMed

Seif, A.E., Barrett, D.M., Milone, M., Brown, V.I., Grupp, S.A., and Reid, G.S. (2009). Long-term protection from syngeneic acute lymphoblastic leukemia by CpG ODN-mediated stimulation of innate and adaptive immune responses. Blood 114, 2459–2466.10.1182/blood-2009-02-203984Search in Google Scholar PubMed PubMed Central

Sidis, Y., Schneyer, A.L., Sluss, P.M., Johnson, L.N., and Keutmann, H.T. (2001). Follistatin: essential role for the N-terminal domain in activin binding and neutralization. J. Biol. Chem. 276, 17718–17726.10.1074/jbc.M100736200Search in Google Scholar PubMed

Stassen, M., Arnold, M., Hultner, L., Muller, C., Neudorfl, C., Reineke, T., and Schmitt, E. (2000). Murine bone marrow-derived mast cells as potent producers of IL-9: costimulatory function of IL-10 and kit ligand in the presence of IL-1. J. Immunol. 164, 5549–5555.10.4049/jimmunol.164.11.5549Search in Google Scholar PubMed

Stassen, M., Muller, C., Arnold, M., Hultner, L., Klein-Hessling, S., Neudorfl, C., Reineke, T., Serfling, E., and Schmitt, E. (2001). IL-9 and IL-13 production by activated mast cells is strongly enhanced in the presence of lipopolysaccharide: NF-B is decisively involved in the expression of IL-9. J. Immunol. 166, 4391–4398.10.4049/jimmunol.166.7.4391Search in Google Scholar PubMed

Talotta, R., Berzi, A., Doria, A., Batticciotto, A., Ditto, M.C., Atzeni, F., Sarzi-Puttini, P., and Trabattoni, D. (2017). The immunogenicity of branded and biosimilar infliximab in rheumatoid arthritis according to Th9-related responses. Int. J. Mol. Sci. 18, pii: E2127.10.3390/ijms18102127Search in Google Scholar PubMed PubMed Central

Tamiya, T., Ichiyama, K., Kotani, H., Fukaya, T., Sekiya, T., Shichita, T., Honma, K., Yui, K., Matsuyama, T., Nakao, T., et al. (2013). Smad2/3 and IRF4 play a cooperative role in IL-9-producing T cell induction. J. Immunol. 191, 2360–2371.10.4049/jimmunol.1301276Search in Google Scholar PubMed

Tang, P.M., Zhou, S., Meng, X.M., Wang, Q.M., Li, C.J., Lian, G.Y., Huang, X.R., Tang, Y.J., Guan, X.Y., Yan, B.P., et al. (2017). Smad3 promotes cancer progression by inhibiting E4BP4-mediated NK cell development. Nat. Commun. 8, 14677.10.1038/ncomms14677Search in Google Scholar PubMed PubMed Central

Thompson, T.B., Lerch, T.F., Cook, R.W., Woodruff, T.K., and Jardetzky, T.S. (2005). The structure of the follistatin:activin complex reveals antagonism of both type I and type II receptor binding. Dev. Cell 9, 535–543.10.1016/j.devcel.2005.09.008Search in Google Scholar PubMed

Vanherberghen, B., Olofsson, P.E., Forslund, E., Sternberg-Simon, M., Khorshidi, M.A., Pacouret, S., Guldevall, K., Enqvist, M., Malmberg, K.J., Mehr, R., et al. (2013). Classification of human natural killer cells based on migration behavior and cytotoxic response. Blood 121, 1326–1334.10.1182/blood-2012-06-439851Search in Google Scholar PubMed

Wang, S.Y., Tai, G.X., Zhang, P.Y., Mu, D.P., Zhang, X.J., and Liu, Z.H. (2008). Inhibitory effect of activin A on activation of lipopolysaccharide-stimulated mouse macrophage RAW264.7 cells. Cytokine 42, 85–91.10.1016/j.cyto.2008.01.010Search in Google Scholar PubMed

Wang, Z.J., Martin, J.A., Gancarz, A.M., Adank, D.N., Sim, F.J., and Dietz, D.M. (2017). Activin A is increased in the nucleus accumbens following a cocaine binge. Sci. Rep. 7, 43658.10.1038/srep43658Search in Google Scholar PubMed PubMed Central

Yadi, H., Burke, S., Madeja, Z., Hemberger, M., Moffett, A., and Colucci, F. (2008). Unique receptor repertoire in mouse uterine NK cells. J. Immunol. 181, 6140–6147.10.4049/jimmunol.181.9.6140Search in Google Scholar PubMed

Yasuda, K., Nakanishi, K., and Tsutsui, H. (2019). Interleukin-18 in health and disease. Int. J. Mol. Sci. 20, pii: E649.10.3390/ijms20030649Search in Google Scholar PubMed PubMed Central

Ying, X., Su, Z., Bie, Q., Zhang, P., Yang, H., Wu, Y., Xu, Y., Wu, J., Zhang, M., Wang, S., et al. (2016). Synergistically increased ILC2 and Th9 cells in lung tissue jointly promote the pathological process of asthma in mice. Mol. Med. Rep. 13, 5230–5240.10.3892/mmr.2016.5174Search in Google Scholar PubMed

Yu, J., Freud, A.G., and Caligiuri, M.A. (2013). Location and cellular stages of natural killer cell development. Trends Immunol. 34, 573–582.10.1016/j.it.2013.07.005Search in Google Scholar PubMed PubMed Central

Zhang, Y., Qi, Y., Zhao, Y., Sun, H., Ge, J., and Liu, Z. (2018). Activin A induces apoptosis of mouse myeloma cells via the mitochondrial pathway. Oncol. Lett. 15, 2590–2594.10.3892/ol.2017.7584Search in Google Scholar PubMed PubMed Central