Betaglycan (TβRIII) Is Expressed in the Thymus and Regulates T Cell Development by Protecting Thymocytes from Apoptosis

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Aleman Muench, German R ^a   Mendoza, Valentin ^b   Stenvers, Kaye ^c   Garcia Zepeda, Eduardo A ^a   Lopez Casillas, Fernando ^b   Raman, Chander ^d   Soldevila, Gloria ^a  

^a INSTITUTO DE INVESTIGACIONES BIOMÉDICAS   (Mexico)

^b INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

^c HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d The University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INHIBIN A; MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 3;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; IN VITRO STUDY; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; ONTOGENY; STROMA CELL; T LYMPHOCYTE; THYMOCYTE; THYMUS;

ANIMALS; APOPTOSIS; CYTOPROTECTION; EMBRYO, MAMMALIAN; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, INBRED C57BL; ORGAN CULTURE TECHNIQUES; PROTEOGLYCANS; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA, MESSENGER; STROMAL CELLS; T-LYMPHOCYTES; THYMOCYTES; THYMUS GLAND;

EID: 84865610415     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044217     Document Type: Article

References (40)

1. Massague J, (1990) The transforming growth factor-beta family. Annu Rev Cell Biol 6: 597-641.
2. Chen YG, Wang Q, Lin SL, Chang CD, Chuang J, Ying SY, (2006) Activin signaling and its role in regulation of cell proliferation, apoptosis, and carcinogenesis. Exp Biol Med (Maywood) 231: 534-544.
3. Ten Dijke P, Goumans MJ, Itoh F, Itoh S, (2002) Regulation of cell proliferation by Smad proteins. J Cell Physiol 191: 1-16.
4. Licona-Limon P, Soldevila G, (2007) The role of TGF-beta superfamily during T cell development: new insights. Immunol Lett 109: 1-12.
5. Varas A, Hager-Theodorides AL, Sacedon R, Vicente A, Zapata AG, et al. (2003) The role of morphogens in T-cell development. Trends Immunol 24: 197-206.
6. Licona P, Chimal-Monroy J, Soldevila G, (2006) Inhibins are the major activin ligands expressed during early thymocyte development. Dev Dyn 235: 1124-1132.
7. Licona-Limon P, Aleman-Muench G, Chimal-Monroy J, Macias-Silva M, Garcia-Zepeda EA, et al. (2009) Activins and inhibins: novel regulators of thymocyte development. Biochem Biophys Res Commun 381: 229-235.
8. Mythreye K, Blobe GC, (2009) The type III TGFbeta receptor regulates directional migration: new tricks for an old dog. Cell Cycle 8: 3069-3070.
9. Gatza CE, Oh SY, Blobe GC, (2010) Roles for the type III TGF-beta receptor in human cancer. Cellular signalling 22: 1163-1174.
10. Stenvers KL, Tursky ML, Harder KW, Kountouri N, Amatayakul-Chantler S, et al. (2003) Heart and liver defects and reduced transforming growth factor beta2 sensitivity in transforming growth factor beta type III receptor-deficient embryos. Mol Cell Biol 23: 4371-4385.
11. Sarraj MA, Escalona RM, Umbers A, Chua HK, Small C, et al. (2010) Fetal testis dysgenesis and compromised Leydig cell function in Tgfbr3 (beta glycan) knockout mice. Biology of reproduction 82: 153-162.
12. Walker KA, Sims-Lucas S, Caruana G, Cullen-McEwen L, Li J, et al. (2011) Betaglycan is required for the establishment of nephron endowment in the mouse. PLoS One 6: e18723.
13. Lopez-Casillas F, Wrana JL, Massague J, (1993) Betaglycan presents ligand to the TGF beta signaling receptor. Cell 73: 1435-1444.
14. Esparza-Lopez J, J. L Montiel, M. M Vilchis-Landeros, T Okadome, K Miyazono, Lopez-Casillas F, (2001) Ligand binding and functional properties of betaglycan, a co-receptor of the transforming growth factor-beta superfamily. Specialized binding regions for transforming growth factor-beta and inhibin A. J Biol Chem 276: 14588-14596.
15. Lopez-Casillas F, Riquelme C, Perez-Kato Y, Ponce-Castaneda MV, Osses N, et al. (2003) Betaglycan expression is transcriptionally up-regulated during skeletal muscle differentiation. Cloning of murine betaglycan gene promoter and its modulation by MyoD, retinoic acid, and transforming growth factor-beta. J Biol Chem 278: 382-390.
16. Sankar S, Mahooti-Brooks N, (1995) Centrella M, McCarthy TL, Madri JA (1995) Expression of transforming growth factor type III receptor in vascular endothelial cells increases their responsiveness to transforming growth factor beta 2. J Biol Chem 270: 13567-13572.
17. Brown CB, Boyer AS, Runyan RB, Barnett JV, (1999) Requirement of type III TGF-beta receptor for endocardial cell transformation in the heart. Science 283: 2080-2082.
18. Kirkbride KC, Townsend TA, Bruinsma MW, Barnett JV, Blobe GC, (2008) Bone morphogenetic proteins signal through the transforming growth factor-beta type III receptor. J Biol Chem 283: 7628-7637.
19. Stenvers KL, (2010) Findlay (2010) Inhibins: from reproductive hormones to tumor suppressors. Trends in endocrinology and metabolism: TEM 21: 174-180.
20. Lewis KA, Gray PC, Blount AL, MacConell LA, Wiater E, et al. (2000) Betaglycan binds inhibin and can mediate functional antagonism of activin signalling. Nature 404: 411-414.
21. Chapman SC, Bernard DJ, Jelen J, Woodruff TK, (2002) Properties of inhibin binding to betaglycan, InhBP/p120 and the activin type II receptors. Mol Cell Endocrinol 196: 79-93.
22. Wiater E, Vale W, (2003) Inhibin is an antagonist of bone morphogenetic protein signaling. J Biol Chem 278: 7934-7941.
23. Looyenga BD, Wiater E, Vale W, Hammer GD, (2010) Inhibin-A antagonizes TGFbeta2 signaling by down-regulating cell surface expression of the TGFbeta coreceptor betaglycan. Mol Endocrinol 24: 608-620.
24. Farnworth PG, Wang Y, Escalona R, Leembruggen P, Ooi GT, et al. (2007) Transforming growth factor-beta blocks inhibin binding to different target cell types in a context-dependent manner through dual mechanisms involving betaglycan. Endocrinology 148: 5355-5368.
25. Ethier JF, Farnworth PG, Findlay JK, Ooi GT, (2002) Transforming growth factor-beta modulates inhibin A bioactivity in the LbetaT2 gonadotrope cell line by competing for binding to betaglycan. Mol Endocrinol 16: 2754-2763.
26. Kadin ME, Cavaille-Coll MW, Gertz R, Massague J, Cheifetz S, et al. (1994) Loss of receptors for transforming growth factor beta in human T-cell malignancies. Proc Natl Acad Sci U S A 91: 6002-6006.
27. Pakula R, Melchior A, Denys A, Vanpouille C, Mazurier J, et al. (2007) Syndecan-1/CD147 association is essential for cyclophilin B-induced activation of p44/42 mitogen-activated protein kinases and promotion of cell adhesion and chemotaxis. Glycobiology 17: 492-503.
28. Buckham Sporer KR, Burton JL, Earley B, Crowe MA, (2007) Transportation stress in young bulls alters expression of neutrophil genes important for the regulation of apoptosis, tissue remodeling, margination, and anti-bacterial function. Vet Immunol Immunopathol 118: 19-29.
29. Brooks SP, Bernstein ZP, Schneider SL, Gollnick SO, Tomasi TB, (1998) Role of transforming growth factor-beta1 in the suppressed allostimulatory function of AIDS patients. Aids 12: 481-487.
30. Slimani H, Charnaux N, Mbemba E, Saffar L, Vassy R, et al. (2003) Interaction of RANTES with syndecan-1 and syndecan-4 expressed by human primary macrophages. Biochim Biophys Acta 1617: 80-88.
31. Schick BP, Jacoby JA, (1995) Serglycin and betaglycan proteoglycans are expressed in the megakaryocytic cell line CHRF 288-11 and normal human megakaryocytes. J Cell Physiol 165: 96-106.
32. Sarraj MA, Chua HK, Umbers A, Loveland KL, Findlay JK, et al. (2007) Differential expression of TGFBR3 (betaglycan) in mouse ovary and testis during gonadogenesis. Growth Factors 25: 334-345.
33. Rosendahl A, Speletas M, Leandersson K, Ivars F, Sideras P, (2003) Transforming growth factor-beta- and Activin-Smad signaling pathways are activated at distinct maturation stages of the thymopoeisis. Int Immunol 15: 1401-1414.
34. Graf D, Nethisinghe S, Palmer DB, Fisher AG, Merkenschlager M, (2002) The developmentally regulated expression of Twisted gastrulation reveals a role for bone morphogenetic proteins in the control of T cell development. J Exp Med 196: 163-171.
35. Stenvers KL, Findlay JK, (2010) Inhibins: from reproductive hormones to tumor suppressors. Trends Endocrinol Metab 21: 174-180.
36. Chu W, Li X, Li C, Wan L, Shi H, et al. (2011) TGFBR3, a potential negative regulator of TGF-beta signaling, protects cardiac fibroblasts from hypoxia-induced apoptosis. J Cell Physiol 226: 2586-2594.
37. Mythreye K, Blobe GC, (2009) The type III TGF-beta receptor regulates epithelial and cancer cell migration through beta-arrestin2-mediated activation of Cdc42. Proc Natl Acad Sci U S A 106: 8221-8226.
38. Margulis V, Maity T, Zhang XY, Cooper SJ, Copland JA, et al. (2008) Type III transforming growth factor-beta (TGF-beta) receptor mediates apoptosis in renal cell carcinoma independent of the canonical TGF-beta signaling pathway. Clin Cancer Res 14: 5722-5730.
39. Blair CR, Stone JB, Wells RG, (2011) The type III TGF-beta receptor betaglycan transmembrane-cytoplasmic domain fragment is stable after ectodomain cleavage and is a substrate of the intramembrane protease gamma-secretase. Biochimica et biophysica acta 1813: 332-339.
40. Yuan JS, Kousis PC, Suliman S, Visan I, Guidos CJ, (2010) Functions of notch signaling in the immune system: consensus and controversies. Annual review of immunology 28: 343-365.