Activin-A: A novel critical regulator of allergic asthma

Clinical and Experimental Allergy

Volumn 41, Issue 11, 2011, Pages 1505-1514

  Kariyawasam, H H ^a   Semitekolou, M ^b   Robinson, D S ^c,d   Xanthou, G ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b BIOMEDICAL RESEARCH FOUNDATION   (Greece)

^c NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^d Laboratorios Leti SL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; ALLERGEN; CYTOKINE; TRANSFORMING GROWTH FACTOR BETA;

ALLERGIC ASTHMA; ANTIINFLAMMATORY ACTIVITY; HUMAN; IMMUNITY; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RESPIRATORY EPITHELIUM; REVIEW; TH2 CELL;

ACTIVINS; AIRWAY REMODELING; ANIMALS; ASTHMA; CYTOKINES; HUMANS; INFLAMMATION; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 80054043793     PISSN: 09547894     EISSN: 13652222     Source Type: Journal    
DOI: 10.1111/j.1365-2222.2011.03784.x     Document Type: Review

References (80)

1. Holgate ST. Has the time come to rethink the pathogenesis of asthma? Curr Opin Allergy Clin Immunol 2010; 10:48-53. Review.
2. Ryanna K, Stratigou V, Safinia N, Hawrylowicz C. Regulatory T cells in bronchial asthma. Allergy 2009; 64:335-47.
3. Robinson DS. The Role of the T cell in asthma. J Allergy Clin Immunol 2010; 126:1081-91.
4. Wang YH, Voo KS, Liu Bet al. A novel subset of CD4(+) T(H)2 memory/effector cells that produce inflammatory IL-17 cytokine and promote the exacerbation of chronic allergic asthma. J Exp Med 2010; 207:2479-91.
5. Eberl G. Immunology: close encounters of the second type. Nature 2010; 464:1285-6.
6. Lloyd CM, Hawrylowicz CM. Regulatory T cells in asthma. Immunity 2009; 31:438-49.
7. Thorburn AN, Hansbro PM. Harnessing regulatory T cells to suppress asthma: from potential to therapy. Am J Respir Cell Mol Biol 2010; 43:511-9.
8. Xia Y, Schneyer AL. The biology of activin: recent advances in structure, regulation and function. J Endocrinol 2009; 202:1-12. Review.
9. Kitisin K, Saha T, Blake Tet al. TGF-beta signaling in development. Sci STKE 2007; 399, DOI: DOI: 10.1126/stke.3992007cm1.
10. Ling N, Ying SY, Ueno Net al. A homodimer of the beta-subunits of inhibin A stimulates the secretion of pituitary follicle stimulating hormone. Biochem Biophys Res Commun 1986; 138:1129-37.
11. Matzuk MM, Bradley A. Functional analysis of activins during mammalian development. Nature 1995; 374:354-6.
12. Matzuk MM, Kumar TR, Bradley A. Different phenotypes for mice deficient in either activins or activin receptor type II. Nature 1995; 374:356-60.
13. Woodruff TK. Regulation of cellular and system function by activin. Biochem Pharmacol 1998; 55:953-63.
14. Mason AJ, Farnworth PG, Sullivan J. Characterization and determination of the biological activities of noncleavable high molecular weight forms of inhibin A and activin A. Mol Endocrinol 1996; 10:1055-65.
15. Piek E, Heldin CH, ten Dijke P. Specificity, diversity, and regulation in TGF-beta superfamily signalling 720. FASEB J 1999; 13:2105-24.
16. Harrison CA, Gray PC, Vale WW, Robertson DM. Antagonists of activin signaling: mechanisms and potential biological applications. Trends Endocrinol Metab 2005; 16:73-8.
17. Iemura S, Yamamoto TS, Takagi Cet al. 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 1998; 95:9337-42.
18. Nogai H, Rosowski M, Grün Jet al. Follistatin antagonizes transforming growth factor-beta3-induced epithelial-mesenchymal transition in vitro: implications for murine palatal development supported by microarray analysis. Differentiation 2008; 76:404-16.
19. Afrakhte M, Moren A, Jossan Set al. Induction of inhibitory Smad6 and Smad7 mRNA by TGF-beta family members. Biochem Biophys Res Commun 1998; 249:505-11.
20. Bitzer M, von Gersdorff G, Liang Det al. A mechanism of suppression of TGF-beta/SMAD signaling by NF-kappa B/RelA. Genes Dev 2000; 14:187-97.
21. Ulloa L, Doody J, Massagué J. Inhibition of transforming growth factor-beta/SMAD signalling by the interferon-gamma/STAT pathway. Nature 1999; 397:710-3.
22. Ogawa K, Funaba M, Mathews LS, Mizutani T. Activin A stimulates type IV collagenase (matrix metalloproteinase-2) production in mouse peritoneal macrophages. J Immunol 2000; 165:2997-3003.
23. Abe M, Shintani Y, Eto Y, Harada K, Kosaka M, Matsumoto T. Potent induction of activin A secretion from monocytes and bone marrow stromal fibroblasts by cognate interaction with activated T cells. J Leukoc Biol 2002; 72:347-52.
24. Robson NC, Phillips DJ, McAlpine Tet al. Activin-A: a novel dendritic cell-derived cytokine that potently attenuates CD40 ligand-specific cytokine and chemokine production. Blood 2008; 111:2733-43.
25. Phillips DJ, de Kretser DM, Hedger MP. Activin and related proteins in inflammation: not just interested bystanders. Cytokine Growth Factor Rev 2009; 20:153-64. Review.
26. Shao L, Frigon NLJr, Sehy DWet al. Regulation of production of activin A in human marrow stromal cells and monocytes. Exp Hematol 1992; 20:1235-42.
27. Yu EW, Dolter KE, Shao LE, Yu J. Suppression of IL-6 biological activities by activin A and implications for inflammatory arthropathies. Clin Exp Immunol 1998; 12:126-32.
28. Jones KL, Brauman JN, Groome NP, de Kretser DM, Phillips DJ. Activin A release into the circulation is an early event in systemic inflammation and precedes the release of follistatin. Endocrinology 2000; 141:1905-8.
29. Jones KL, de Kretser DM, Clarke IJ, Scheerlinck JP, Phillips DJ. Characterisation of the rapid release of activin A following acute lipopolysaccharide challenge in the ewe. J Endocrinol 2004; 182:69-80.
30. Jones KL, de Kretser DM, Patella S, Phillips DJ. Activin A and follistatin in systemic inflammation. Mol Cell Endocrinol 2004; 225:119-25. Review.
31. Dohi T, Ejima C, Kato Ret al. Therapeutic potential of follistatin for colonic inflammation in mice. Gastroenterology 2005; 128:411-23.
32. Hubner G, Brauchle M, Gregor M, Werner S. Activin A: a novel player and inflammatory marker in inflammatory bowel disease? Lab Invest 1997; 77311-8.
33. Ota F, Maeshima A, Yamashita Set al. Activin A induces cell proliferation of fibroblast-like synoviocytes in rheumatoid arthritis. Arthritis Rheum 2003; 48:2442-9.
34. Hübner G, Alzheimer C, Werner S. Activin: a novel player in tissue repair processes. Histol Histopathol 1999; 14:295-304. Review.
35. Matsuse T, Fukuchi Y, Eto Yet al. Expression of immunoreactive and bioactive activin A protein in adult murine lung after bleomycin treatment. Am J Respir Cell Mol Biol 1995; 13:17-24.
36. Matsuse T, Ikegami A, Ohga Eet al. Expression of immunoreactive activin A protein in remodeling lesions associated with interstitial pulmonary fibrosis. Am J Pathol 1996; 148:707-13.
37. Ohga E, Matsuse T, Teramoto Set al. Effects of activin A on proliferation and differentiation of human lung fibroblasts. Biochem Biophys Res Commun 1996; 228:391-6.
38. Aoki F, Kurabayashi M, Hasegawa Y, Kojima I. Attenuation of bleomycin-induced pulmonary fibrosis by follistatin. Am J Respir Crit Care Med 2005; 172:713-20.
39. Takagi K, Kawaguchi Y, Kawamoto Met al. Activation of the activin A-ALK-Smad pathway in systemic sclerosis. J Autoimmun 2011; 36: 181-8.
40. Hedger MP, Winnall WR, Phillips DJ, de Kretser DM. The regulation and functions of activin and follistatin in inflammation and immunity. Vitam Horm 2011; 85:255-97.
41. Nüsing RM, Barsig J. Induction of prostanoid, nitric oxide, and cytokine formation in rat bone marrow derived macrophages by activin A. Br J Pharmacol 1999; 127:919-26.
42. Wang Y, Cui X, Tai Get al. A critical role of activin A in maturation of mouse peritoneal macrophages in vitro and in vivo. Cell Mol Immunol 2009; 6:387-92.
43. Musso T, Scutera S, Vermi Wet al. Activin A induces Langerhans cell differentiation in vitro and in human skin explants. PLoS One 2008; 3:e3271.
44. Salogni L, Musso T, Bosisio Det al. Activin A induces dendritic cell migration through the polarized release of CXC chemokine ligands 12 and 14. Blood 2009; 113:5848-56.
45. Ogawa K, Funaba M, Tsujimoto M.A dual role of activin A in regulating immunoglobulin production of B cells. J Leukoc Biol 2008; 83:1451-8.
46. Ogawa K, Funaba M. Activin in humoral immune responses. Vitam Horm 2011; 85:235-53.
47. Sierra-Filardi E, Puig-Kröger A, Blanco FJet al. Activin A skews macrophage polarization by promoting a pro-inflammatory phenotype and inhibiting the acquisition of anti-inflammatory macrophage markers. Blood 2011. DOI: DOI: 10.1182/blood-2010-09-306993.
48. Jones KL, Mansell A, Patella Set al. Activin A is a critical component of the inflammatory response, and its binding protein, follistatin, reduces mortality in endotoxemia. Proc Natl Acad Sci USA 2007; 104:16239-44.
49. Hedger MP, Drummond AE, Robertson DM, Risbridger GP, de Kretser DM. Inhibin and activin regulate [3H]thymidine uptake by rat thymocytes and 3T3 cells in vitro. Mol Cell Endocrinol 1989; 61:133-8.
50. Wang SY, Tai GX, Zhang PY, Mu DP, Zhang XJ, Liu ZH. Inhibitory effect of activin A on activation of lipopolysaccharide-stimulated mouse macrophage RAW264 7 cells. Cytokine 2008; 42:85-91.
51. Zhou J, Tai G, Liu Het al. Activin A down-regulates the phagocytosis of lipopolysaccharide-activated mouse peritoneal macrophages in vitro and in vivo. Cell Immunol 2009; 255:69-75.
52. Brosh N, Sternberg D, Honigwachs-Sha'anani Jet al. 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 1995; 270:29594-600.
53. Lee HJ, Kim PH. Further characterization of activin A-induced IgA response in murine B lymphocytes. Immune Netw 2009; 9:133-7.
54. Segerer SE, Müller N, Brandt Jet al. The glycoprotein-hormones activin A and inhibin A interfere with dendritic cell maturation. Reprod Biol Endocrinol 2008; 6:17.
55. Della Bella S, Giannelli S, Cozzi Vet al. Incomplete activation of peripheral blood dendritic cells during healthy human pregnancy. Clin Exp Immunol 2011; 164:180-92.
56. Robson NC, Wei H, McAlpine T, Kirkpatrick N, Cebon J, Maraskovsky E. Activin-A attenuates several human natural killer cell functions. Blood 2009; 113:3218-25.
57. Bonfield TL, Barna BP, John Net al. Suppression of activin A in autoimmune lung disease associated with anti-GM-CSF. J Autoimmun 2006; 26:37-41.
58. Huber S, Stahl FR, Schrader Jet al. Activin a promotes the TGF-beta-induced conversion of CD4+ CD25- T cells into Foxp3+ induced regulatory T cells. J Immunol 2009; 182:4633-40.
59. Rosendahl A, Checchin D, Fehniger TE, ten Dijke P, Heldin CH, Sideras P. Activation of the TGF-beta/activin-Smad2 pathway during allergic airway inflammation. Am J Respir Cell Mol Biol 2001; 25:60-8.
60. Cho SH, Yao Z, Wang SWet al. Regulation of activin A expression in mast cells and asthma: its effect on the proliferation of human airway smooth muscle cells. J Immunol 2003; 170:4045-52.
61. Brightling CE, Bradding P, Symon FA, Holgate ST, Wardlaw AJ, Pavord ID. Mast-cell infiltration of airway smooth muscle in asthma. N Engl J Med 2002; 346:1699-705.
62. Funaba M, Ikeda T, Ogawa K, Murakami M, Abe M. Role of activin A in murine mast cells: modulation of cell growth, differentiation, and migration. J Leukoc Biol 2003; 73:793-801.
63. Ogawa K, Funaba M, Chen Y, Tsujimoto M. Activin A functions as a Th2 cytokine in the promotion of the alternative activation of macrophages. J Immunol 2006; 177:6787-94.
64. Hardy CL, O'Connor AE, Yao Jet al. Follistatin is a candidate endogenous negative regulator of activin A in experimental allergic asthma. Clin Exp Allergy 2006; 36:941-50.
65. Semitekolou M, Alissafi T, Aggelakopoulou Met al. Activin-A induces regulatory T cells that suppress T helper cell immune responses and protect from allergic airway disease. J Exp Med 2009; 206:1769-85.
66. Gregory LG, Mathie SA, Walker SA, Pegorier S, Jones CP, Lloyd CM. Overexpression of Smad2 drives house dust mite-mediated airway remodeling and airway hyperresponsiveness via activin and IL-25. Am J Respir Crit Care Med 2010; 182:143-54.
67. Hardy CL, Lemasurier JS, Olsson Fet al. Interleukin-13 regulates secretion of the tumor growth factor-{beta} superfamily cytokine activin A in allergic airway inflammation. Am J Respir Cell Mol Biol 2010; 42:667-75.
68. Von Bubnoff D, Matz H, Cazenave JP, Hanau D, Bieber T, De La Salle H. Kinetics of gene induction after FcepsilonRI ligation of atopic monocytes identified by suppression subtractive hybridization. J Immunol 2002; 169:6170-7.
69. Karagiannidis C, Hense G, Martin Cet al. Activin A is an acute allergen-responsive cytokine and provides a link to TGF-beta-mediated airway remodeling in asthma. J Allergy Clin Immunol 2006; 117:111-8.
70. Kariyawasam HH, Pegorier S, Barkans Jet al. Activin and transforming growth factor-beta signaling pathways are activated after allergen challenge in mild asthma. J Allergy Clin Immunol 2009; 124:454-62.
71. Chen Y, Wu H, Winnall WRet al. Tumour necrosis factor-α stimulates human neutrophils to release preformed activin A. Immunol Cell Biol 2011. DOI: DOI: 10.1038/icb.2011.12.
72. Wenzel SE. Asthma: defining of the persistent adult phenotypes. Lancet 2006; 368:804-13. Review.
73. Leigh R, Oyelusi W, Wiehler Set al. Human rhinovirus infection enhances airway epithelial cell production of growth factors involved in airway remodeling. J Allergy Clin Immunol 2008; 121:1238-45.
74. Sagara H, Okada T, Okumura Ket al. Activation of TGF-beta/Smad2 signaling is associated with airway remodeling in asthma. J Allergy Clin Immunol 2002; 110:249-54.
75. Nakao A, Sagara H, Setoguchi Yet al. Expression of Smad7 in bronchial epithelial cells is inversely correlated to basement membrane thickness and airway hyperresponsiveness in patients with asthma. J Allergy Clin Immunol 2002; 110:873-8.
76. Khalil N, Parekh TV, O'Connor RN, Gold LI. Differential expression of transforming growth factor-beta type I and II receptors by pulmonary cells in bleomycin-induced lung injury: correlation with repair and fibrosis. Exp Lung Res 2002; 28:233-50.
77. Hammad H, Chieppa M, Perros F, Willart MA, Germain RN, Lambrecht BN. House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells. Nat Med 2009; 15:410-6.
78. Phipps S, Benyahia F, Ou TT, Barkans J, Robinson DS, Kay AB. Acute allergen-induced airway remodeling in atopic asthma. Am J Respir Cell Mol Biol 2004; 31:626-32.
79. Torrego A, Hew M, Oates T, Sukkar M, Fan CK. Expression and activation of TGF-beta isoforms in acute allergen-induced remodelling in asthma. Thorax 2007; 62:307-13.
80. Kariyawasam HH, Aizen M, Barkans J, Robinson DS, Kay AB. Remodeling and airway hyperresponsiveness but not cellular inflammation persist after allergen challenge in asthma. Am J Respir Crit Care Med 2007; 175:896-904.