Activin and related proteins in inflammation: Not just interested bystanders

McDowall, 2008, The role of activins and follistatins in skin and hair follicle development and function, Cytokine Growth Factor Rev, 19, 415, 10.1016/j.cytogfr.2008.08.005 Phillips, 2003, The activin/inhibin family, vol. 2, 1153 Robertson, 1992, Inhibin/activin β-subunit monomer: isolation and characterization, Endocrinology, 130, 1680, 10.1210/en.130.3.1680 Brown, 2000, Insertion of Inhbb into the Inhba locus rescues the Inhba-null phenotype and reveals new activin functions, Nat Genet, 25, 453, 10.1038/78161 Muenster, 2005, An activin-A/C chimera exhibits activin and myostatin antagonistic properties, J Biol Chem, 280, 36626, 10.1074/jbc.M507236200 Phillips, 1998, Follistatin: a multifunctional regulatory protein, Front Neuroendocrinol, 19, 287, 10.1006/frne.1998.0169 Lerch, 2007, Structural and biophysical coupling of heparin and activin binding to follistatin isoform functions, J Biol Chem, 282, 15930, 10.1074/jbc.M700737200 Stamler, 2008, The structure of FSTL3:activin A complex: differential binding of N-terminal domains influences follistatin-type antagonist specificity, J Biol Chem, 283, 32831, 10.1074/jbc.M801266200 Iemura, 1998, Direct binding of follistatin to a complex of bone-morphogenetic protein and its receptor inhibits ventral and epidermal cell fates in early Xenopus embryo, Proc Natl Acad Sci USA, 95, 9337, 10.1073/pnas.95.16.9337 Phillips, 1996, Follistatin concentrations in male sheep increase following sham castration/castration or injection of interleukin-1β, J Endocrinol, 151, 119, 10.1677/joe.0.1510119 Klein, 1996, Plasma follistatin concentrations increase following lipopolysaccharide administration in sheep, Clin Exp Pharmacol Physiol, 23, 754, 10.1111/j.1440-1681.1996.tb01773.x Phillips, 1998, Follistatin has a biphasic response but follicle-stimulating hormone is unchanged during an inflammatory episode in growing lambs, J Endocrinol, 156, 77, 10.1677/joe.0.1560077 Jones, 2000, Activin A release into the circulation is an early event in systemic inflammation and precedes the release of follistatin, Endocrinology, 141, 1905, 10.1210/en.141.5.1905 Jones, 2004, Characterisation of the rapid release of activin A following acute lipopolysaccharide challenge in the ewe, J Endocrinol, 182, 69, 10.1677/joe.0.1820069 McClure, 2005, Effects of age and pregnancy on the circulatory activin response of sheep to acute inflammatory challenge by lipopolysaccharide, J Endocrinol, 185, 139, 10.1677/joe.1.06051 Jones, 2007, Activin A is a critical component of the inflammatory response, and its binding protein, follistatin, reduces mortality in endotoxemia, Proc Natl Acad Sci USA, 104, 16239, 10.1073/pnas.0705971104 Rifkin, 2005, Latent transforming growth factor-β (TGF-β) binding proteins: orchestrators of TGF-β availability, J Biol Chem, 280, 7409, 10.1074/jbc.R400029200 Sakai, 1992, The measurement of activin/EDF in mouse serum: evidence for extragonadal production, Biochem Biophys Res Commun, 188, 921, 10.1016/0006-291X(92)91143-E Erämaa, 1992, Activin A/erythroid differentiation factor is induced during human monocyte activation, J Exp Med, 176, 1449, 10.1084/jem.176.5.1449 Wang, 2008, Inhibitory effect of activin A on activation of lipopolysaccharide-stimulated mouse macrophage RAW264.7 cells, Cytokine, 42, 85, 10.1016/j.cyto.2008.01.010 Robson, 2008, Activin A: a novel dendritic cell derived cytokine which potently attenuates CD40 ligand-specific cytokine and chemokine production, Blood, 111, 2733, 10.1182/blood-2007-03-080994 Wilson, 2006, Stimulatory effects of lipopolysaccharide on endothelial cell activin and follistatin, Mol Cell Endocrinol, 253, 30, 10.1016/j.mce.2006.03.041 Phillips, 2001, Evidence for activin A and follistatin involvement in the systemic inflammatory response, Mol Cell Endocrinol, 180, 155, 10.1016/S0303-7207(01)00516-0 Michel, 2003, Serum concentrations of activin and follistatin are elevated and run in parallel in patients with septicemia, Eur J Endocrinol, 148, 559, 10.1530/eje.0.1480559 Ebert, 2006, Activin A concentrations in human cerebrospinal fluid are age-dependent and elevated in meningitis, J Neurol Sci, 250, 50, 10.1016/j.jns.2006.06.026 Michel, 2003, Increased activin levels in cerebrospinal fluid of rabbits with bacterial meningitis are associated with activation of microglia, J Neurochem, 86, 238, 10.1046/j.1471-4159.2003.01834.x Phillips, 2006, Activin A release into cerebrospinal fluid in a subset of patients with severe traumatic brain injury, J Neurotrauma, 23, 1283, 10.1089/neu.2006.23.1283 McLean, 2008, Temporal expression of activin in acute burn wounds—from inflammatory cells to fibroblasts, Burns, 34, 50, 10.1016/j.burns.2007.01.014 Akira, 2006, Pathogen recognition and innate immunity, Cell, 124, 783, 10.1016/j.cell.2006.02.015 Ebert, 2007, Microglial cells and peritoneal macrophages release activin A upon stimulation with Toll-like receptor agonists, Neurosci Lett, 413, 241, 10.1016/j.neulet.2006.11.065 Dower, 2008, Innate immune responses to TREM-1 activation: overlap, divergence, and positive and negative cross-talk with bacterial lipopolysaccharide, J Immunol, 180, 3520, 10.4049/jimmunol.180.5.3520 Keelan, 1998, Regulation of activin-A production by human amnion, decidua and placenta in vitro by pro-inflammatory cytokines, Placenta, 19, 429, 10.1016/S0143-4004(98)90084-4 Okuma, 2005, Reciprocal regulation of activin A and inhibin B by interleukin-1 (IL-1) and follicle-stimulating hormone (FSH) in rat Sertoli cells in vitro, J Endocrinol, 185, 99, 10.1677/joe.1.06053 Shao, 1992, Regulation of production of activin A in human marrow stromal cells and monocytes, Exp Hematol, 20, 1235 Takahashi, 1992, Tumor necrosis factor and interleukin-1 induce activin A gene expression in a human bone marrow stromal cell line, Biochem Biophys Res Commun, 188, 310, 10.1016/0006-291X(92)92386-C Miyanaga, 1993, Differential control of activin, inhibin and follistatin proteins in cultured rat granulosa cells, Biochem Biophys Res Commun, 194, 253, 10.1006/bbrc.1993.1812 Pawlowski, 1997, Stimulation of activin A expression in rat aortic smooth muscle cells by thrombin and angiotensin II correlates with neointimal formation in vivo, J Clin Invest, 100, 639, 10.1172/JCI119575 Scutera, 2008, Production and function of activin A in human dendritic cells, Eur Cytokine Netw, 19, 60 Yu, 1996, Induced expression of the new cytokine, activin A, in human monocytes: inhibition by glucocorticoids and retinoic acid, Immunology, 88, 368, 10.1046/j.1365-2567.1996.d01-675.x Cho, 2003, Regulation of activin A expression in mast cells and asthma: its effect on the proliferation of human airway smooth muscle cells, J Immunol, 170, 4045, 10.4049/jimmunol.170.8.4045 Ogawa, 2006, Activin A functions as a Th2 cytokine in the promotion of the alternative activation of macrophages, J Immunol, 177, 6787, 10.4049/jimmunol.177.10.6787 Licona, 2006, Inhibins are the major activin ligands expressed during early thymocyte development, Dev Dyn, 235, 1124, 10.1002/dvdy.20707 Murase, 2001, Possible involvement of protein kinases and Smad2 signaling pathways on osteoclast differentiation enhanced by activin A, J Cell Physiol, 188, 236, 10.1002/jcp.1113 Nüsing, 1999, Induction of prostanoid, nitric oxide, and cytokine formation in rat bone marrow derived macrophages by activin A, Br J Pharmacol, 127, 919, 10.1038/sj.bjp.0702626 Sugatani, 2003, Activin A stimulates I κ B-α/NFκB and RANK expression for osteoclast differentiation, but not AKT survival pathway in osteoclast precursors, J Cell Biochem, 90, 59, 10.1002/jcb.10613 Yamashita, 1993, Effects of activin A on IgE synthesis and cytokine production by human peripheral mononuclear cells, Clin Exp Immunol, 94, 214, 10.1111/j.1365-2249.1993.tb06003.x Ohguchi, 1998, Activin A regulates the production of mature interleukin-1β and interleukin-1 receptor antagonist in human monocytic cells, J Interferon Cytokine Res, 18, 491, 10.1089/jir.1998.18.491 Sugama, 2007, Activin as an anti-inflammatory cytokine produced by microglia, J Neuroimmunol, 192, 31, 10.1016/j.jneuroim.2007.08.016 Hedger, 2000, Divergent cell-specific effects of activin-A on thymocyte proliferation stimulated by phytohemagglutinin, and interleukin 1β or interleukin 6 in vitro, Cytokine, 12, 595, 10.1006/cyto.1999.0597 Perrier d’Hauterive, 2005, Human endometrial leukemia inhibitory factor and interleukin-6: control of secretion by transforming growth factor-β-related members, Neuroimmunomodulation, 12, 157, 10.1159/000084848 Keelan, 2000, Activin A exerts both pro- and anti-inflammatory effects on human term gestational tissues, Placenta, 21, 38, 10.1053/plac.1999.0451 Zhang, 2005, Effects of activin A on the activities of the mouse peritoneal macrophages, Cell Mol Immunol, 2, 63 Nüsing, 1995, Activin A and retinoic acid synergize in cyclooxygenase-1 and thromboxane synthase induction during differentiation of J774.1 macrophages, Eur J Biochem, 227, 130, 10.1111/j.1432-1033.1995.tb20368.x Brosh, 1995, The plasmacytoma growth inhibitor restrictin-P is an antagonist of interleukin 6 and interleukin 11. Identification as a stroma-derived activin A, J Biol Chem, 270, 29594, 10.1074/jbc.270.49.29594 Gribi, 2001, Expression of activin A in inflammatory arthropathies, Mol Cell Endocrinol, 180, 163, 10.1016/S0303-7207(01)00517-2 Hübner, 1997, Activin A: a novel player and inflammatory marker in inflammatory bowel disease?, Lab Invest, 77, 311 Sternberg, 1995, Restrictin-P/stromal activin A, kills its target cells via an apoptotic mechanism, Growth Factors, 12, 277, 10.3109/08977199509028966 Yu, 1998, Suppression of IL-6 biological activities by activin A and implications for inflammatory arthropathies, Clin Exp Immunol, 112, 126, 10.1046/j.1365-2249.1998.00522.x Yu, 1997, Production of activin A and its roles in inflammation and hematopoiesis, Cytokines Cell Mol Ther, 3, 169 Broxmeyer, 1988, Selective and indirect modulation of human multipotential and erythroid hematopoietic progenitor cell proliferation by recombinant human activin and inhibin, Proc Natl Acad Sci USA, 85, 9052, 10.1073/pnas.85.23.9052 Hedger, 1993, Isolation of rat blood lymphocytes using a two-step Percoll density gradient. Effect of activin (erythroid differentiation factor) on peripheral T lymphocyte proliferation in vitro, J Immunol Methods, 163, 133, 10.1016/0022-1759(93)90247-5 Hedger, 1989, Inhibin and activin regulate [3H]thymidine uptake by rat thymocytes and 3T3 cells in vitro, Mol Cell Endocrinol, 61, 133, 10.1016/0303-7207(89)90198-6 Rosendahl, 2003, Transforming growth factor-β-and activin-Smad signaling pathways are activated at distinct maturation stages of the thymopoeisis, Int Immunol, 15, 1401, 10.1093/intimm/dxg139 Phillips, 1999, A sensitive and specific in vitro bioassay for activin using a mouse plasmacytoma cell line, MPC-11, J Endocrinol, 162, 111, 10.1677/joe.0.1620111 Ogawa, 2008, A dual role of activin A in regulating immunoglobulin production of B cells, J Leukoc Biol, 83, 1451, 10.1189/jlb.1007710 Segerer, 2008, The glycoprotein-hormones activin A and inhibin A interfere with dendritic cell maturation, Reprod Biol Endocrinol, 6, 17, 10.1186/1477-7827-6-17 Kozaki, 1997, Role of activin-A and follistatin in foam cell formation of THP-1 macrophages, Arterioscler Thromb Vasc Biol, 17, 2389, 10.1161/01.ATV.17.11.2389 Dohi, 2005, Therapeutic potential of follistatin for colonic inflammation in mice, Gastroenterology, 128, 411, 10.1053/j.gastro.2004.11.063 Ota, 2003, Activin A induces cell proliferation of fibroblast-like synoviocytes in rheumatoid arthritis, Arthritis Rheum, 48, 2442, 10.1002/art.11249 Matsuse, 1995, Expression of immunoreactive and bioactive activin A protein in adult murine lung after bleomycin treatment, Am J Respir Cell Mol Biol, 13, 17, 10.1165/ajrcmb.13.1.7541220 Rosendahl, 2001, Activation of the TGF-β/activin-Smad2 pathway during allergic airway inflammation, Am J Respir Cell Mol Biol, 25, 60, 10.1165/ajrcmb.25.1.4396 Hardy, 2006, Follistatin is a candidate endogenous negative regulator of activin A in experimental allergic asthma, Clin Exp Allergy, 36, 941, 10.1111/j.1365-2222.2006.02523.x Le, 2007, Inhibition of allergen-induced Smad 3-deficient mice, J Immunol, 178, 7310, 10.4049/jimmunol.178.11.7310 Wohlfahrt, 2003, T cell phenotype in allergic asthma and atopic dermatitis, Int Arch Allergy Immunol, 131, 272, 10.1159/000072139 Karagiannidis, 2006, Activin A is an acute allergen-responsive cytokine and provides a link to TGF-β-mediated airway remodeling in asthma, J Allergy Clin Immunol, 117, 111, 10.1016/j.jaci.2005.09.017 Smith, 2004, Potential anti-inflammatory role of activin A in acute coronary syndromes, J Am Coll Cardiol, 44, 369, 10.1016/j.jacc.2004.03.069 Yndestad, 2004, Elevated levels of activin A in heart failure. Potential role in myocardial remodeling, Circulation, 109, 1379, 10.1161/01.CIR.0000120704.97934.41 Kayisli, 2004, Endocrine-immune interactions in human endometrium, Ann N Y Acad Sci, 1034, 50, 10.1196/annals.1335.005 Florio, 2007, Interleukin 1β and progesterone stimulate activin A expression and secretion from cultured human endometrial stromal cells, Reprod Sci, 14, 29, 10.1177/1933719106298191 Keelan, 2000, Regulation of activin A, inhibin A, and follistatin production in human amnion and choriodecidual explants by inflammatory mediators, J Soc Gynecol Investig, 7, 291, 10.1016/S1071-5576(00)00065-4 Mohan, 2001, Effects of cytokines and growth factors on the secretion of inhibin A, activin A and follistatin by term placental villous trophoblasts in culture, Eur J Endocrinol, 145, 505, 10.1530/eje.0.1450505 Mangioni, 2005, Effect of activin A on tumor necrosis factor-α/intercellular adhesion molecule-1 pathway in endometrial stromal cells, Eur J Obstet Gynecol Reprod Biol, 123, 218, 10.1016/j.ejogrb.2005.03.017 Leung, 1998, Immunolocalization of inhibin and activin subunits in human endometrium across the menstrual cycle, Hum Reprod, 13, 3469, 10.1093/humrep/13.12.3469 Jones, 2000, Inhibin and activin subunits are differentially expressed in endometrial cells and leukocytes during the menstrual cycle, in early pregnancy and in women using progestin-only contraception, Mol Hum Reprod, 6, 1107, 10.1093/molehr/6.12.1107 Muttukrishna, 1997, Activin A and inhibin A as possible endocrine markers for pre-eclampsia, Lancet, 349, 1285, 10.1016/S0140-6736(96)09264-1 Manuelpillai, 2001, Activin A and activin receptors in gestational tissue from preeclamptic pregnancies, J Endocrinol, 171, 55, 10.1677/joe.0.1710057 Tannetta, 2003, Endothelial cells and peripheral blood mononuclear cells are a potent source of extraplacental activin A in preeclampsia, J Clin Endocrinol Metab, 88, 5995, 10.1210/jc.2002-021924 de Kretser, 2001, Inhibins, activins and follistatin: actions on the testis, Mol Cell Endocrinol, 180, 87, 10.1016/S0303-7207(01)00502-0 O’Bryan, 2005, Cytokine profiles in the testes of rats treated with lipopolysaccharide reveal localized suppression of inflammatory responses, Am J Physiol Regul Integr Comp Physiol, 288, R1744, 10.1152/ajpregu.00651.2004 Okuma, 2005, Regulation of activin A and inhibin B secretion by inflammatory mediators in adult rat Sertoli cell cultures, J Endocrinol, 187, 125, 10.1677/joe.1.06266 Anderson, 1998, Follistatin and activin A production by the male reproductive tract, Hum Reprod, 13, 3319, 10.1093/humrep/13.12.3319 Ochsenkühn, 2006, The relationship between immunosuppressive activity and immunoregulatory cytokines in seminal plasma: influence of sperm autoimmunity and seminal leukocytes, J Reprod Immunol, 71, 57, 10.1016/j.jri.2006.01.002 Liew, 2007, A stereological analysis of the response of spermatogenesis to an acute inflammmatory episode in adult rats, J Androl, 28, 176, 10.2164/jandrol.106.000752 Nakamura, 1990, Activin-binding protein from rat ovary is follistatin, Science, 247, 836, 10.1126/science.2106159 Jones, 2006, TGF-β superfamily expression and actions in the endometrium and placenta, Reproduction, 132, 217, 10.1530/rep.1.01076 Werner, 2006, Roles of activin in tissue repair, fibrosis, and inflammatory disease, Cytokine Growth Factor Rev, 17, 157, 10.1016/j.cytogfr.2006.01.001 Patella, 2006, Follistatin attenuates early liver fibrosis: effects on hepatic stellate cell activation and hepatocyte apoptosis, Am J Physiol Gastrointest Liver Physiol, 290, G137, 10.1152/ajpgi.00080.2005 Aoki, 2005, Attenuation of bleomycin-induced pulmonary fibrosis by follistatin, Am J Respir Crit Care Med, 172, 713, 10.1164/rccm.200412-1620OC