Pregnancy-specific glycoprotein 1 (PSG1) activates TGF-β and prevents dextran sodium sulfate (DSS)-induced colitis in mice

British Dental Journal

Volumn 217, Issue 2, 2014, Pages 348-358

  Blois, S M ^a   Sulkowski, G ^b   Tirado Gonzalez I ^a   Warren, J ^b   Freitag, N ^a   Klapp, B F ^a   Rifkin, D ^c   Fuss, I ^d   Strober, W ^d   Dveksler, G S ^b  

^a HUMBOLDT UNIVERSITY   (Germany)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84908149391     PISSN: 00070610     EISSN: 17417503     Source Type: Journal    
DOI: 10.1038/mi.2013.53     Document Type: Article

References (45)

1. Massague, J., Blain, S.W. & Lo, R.S. TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 103, 295-309 (2000).
2. Li, M.O. & Flavell, R.A. TGF-beta: a master of all T cell trades. Cell 134, 392-404 (2008).
3. Miyazono, K., Hellman, U., Wernstedt, C. & Heldin, C.H. Latent high molecular weight complex of transforming growth factor beta 1. Purification from human platelets and structural characterization. J. Biol. Chem. 263, 6407-6415 (1988).
4. Walton, K.L. et al. Two distinct regions of latency-associated peptide coordinatestabilityofthe latent transforming growth factor-beta1 complex. J. Biol. Chem. 285, 17029-17037 (2010).
5. Jobling, M.F. et al. Isoform-specific activation of latent transforming growth factor beta (LTGF-beta) by reactive oxygen species. Radiat. Res. 166, 839-848 (2006).
6. Munger, J.S. et al. The integrin alphavbeta6binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96, 319-328 (1999).
7. Ribeiro, S.M., Poczatek, M., Schultz-Cherry, S., Villain, M. & Murphy-Ullrich, J.E. The activation sequence of thrombospondin-1 interacts with the latency-associated peptide to regulate activation of latent transforming growth factor-beta. J. Biol. Chem. 274, 13586-13593 (1999).
8. Zhou, G.Q. et al. Highly specific monoclonal antibody demonstrates that pregnancy-specific glycoprotein (PSG) is limited to syncytiotrophoblast in human early and term placenta. Placenta 18, 491-501 (1997).
9. Pluta, M., Hardt, W., Schmidt-Gollwitzer, K. & Schmidt-Gollwitzer, M. Radioimmunoassay of serum SP 1 and HPL in normal and abnormal pregnancies. Arch. Gynecol. 227, 327-336 (1979).
10. Blois, S.M. et al. Early expression of pregnancy-specific glycoprotein 22 (PSG22) by trophoblast cells modulates angiogenesis in mice. Biol. Reprod. 86, 191 (2012).
11. Wu, J.A., Johnson, B.L., Chen, Y., Ha, C.T. & Dveksler, G.S. Murine pregnancy-specific glycoprotein 23 induces the proangiogenic factors transforming-growth factor beta 1and vascularendothelial growth factor a in cell types involved invascular remodelinginpregnancy. Biol. Reprod. 79, 1054-1061 (2008).
12. McLellan, A.S. et al. Structure and evolution of the mouse pregnancy-specific glycoprotein (Psg) gene locus. BMC Genomics 6, 4 (2005).
13. Pihl, K., Larsen, T., Laursen, I., Krebs, L. & Christiansen, M. First trimester maternal serum pregnancy-specific beta-1-glycoprotein (SP1)as a marker of adverse pregnancy outcome. Prenat. Diagn. 29, 1256-1261 (2009).
14. Grudzinskas, J.G., Gordon, Y.B., Menabawey, M., Lee, J.N., Wadsworth, J. & Chard, T. Identification of high-risk pregnancy by the routine measurement of pregnancy-specific beta 1-glycoprotein. Am. J. Obstet. Gynecol. 147, 10-12 (1983).
15. Jones, R.L., Stoikos, C., Findlay, J.K. & Salamonsen, L.A. TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction 132, 217-232 (2006).
16. Andersson, J. et al. CD4 + FoxP3 + regulatory T cells confer infectious tolerance inaTGF-beta-dependent manner. J. Exp. Med. 205, 1975-1981 (2008).
17. Aluvihare, V.R., Kallikourdis, M. & Betz, A.G. Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 5, 266-271 (2004).
18. Letterio, J.J. & Roberts, A.B. Transforming growth factor-beta1-deficient mice: identification of isoform-specific activities in vivo. J. Leukoc. Biol. 59, 769-774 (1996).
19. Lee, Y. et al. Induction and molecular signature of pathogenic TH17 cells. Nat. Immunol. 13, 991-999 (2012).
20. Snyder, S.K. et al. Pregnancy-specific glycoproteins function as immuno-modulators by inducing secretion of IL-10, IL-6 and TGF-beta1 by human monocytes. Am. J. Reprod. Immunol. 45, 205-216 (2001).
21. Martinez, F.F., Knubel, C.P., Sanchez, M.C., Cervi, L. & Motran, C.C. Pregnancy-specific glycoprotein 1a activates dendritic cells to provide signals for Th17-, Th2-, and Treg-cell polarization. Eur. J. Immunol. 42, 1573-1584 (2012).
22. Ha, C.T. et al. Human pregnancy specific beta-1-glycoprotein 1 (PSG1) has a potential role in placental vascular morphogenesis. Biol. Reprod. 83, 27-35 (2010).
23. Kunzmann, S. et al. TGF-beta1 in SP-A preparations influence immune suppressive properties of SP-A on human CD4+ T lymphocytes. Am. J. Physiol. Lung Cell Mol. Physiol. 291, L747-L756 (2006).
24. Tesseur, I. et al. Bioactive TGF-beta can associate with lipoproteins and is enriched in those containing apolipoprotein E3. J. Neurochem. 110, 1254-1262 (2009).
25. Abe, M., Harpel, J.G., Metz, C.N., Nunes, I., Loskutoff, D.J. & Rifkin, D.B. An assay for transforming growth factor-beta using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal. Biochem. 216, 276-284 (1994).
26. Tesseur, I., Zou, K., Berber, E., Zhang, H. & Wyss-Coray, T. Highly sensitive and specific bioassay for measuring bioactive TGF-beta. BMC Cell Biol. 7, 15 (2006).
27. Munger, J.S., Harpel, J.G., Gleizes, P.E., Mazzieri, R., Nunes, I. & Rifkin, D.B. Latent transforming growth factor-beta: structural features and mechanisms of activation. Kidney Int. 51, 1376-1382 (1997).
28. Strober, W., Fuss, I.J. & Blumberg, R.S. The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 20, 495-549 (2002).
29. Boirivant, M. et al. Inhibition of Smad7 with a specific antisense oligonucleotide facilitates TGF-beta1-mediated suppression of colitis. Gastroenterology 131, 1786-1798 (2006).
30. Travis, M.A. et al. Loss of integrin alpha(v)beta8 on dendritic cells causes autoimmunity and colitis in mice. Nature 449, 361-365 (2007).
31. Lacy-Hulbert, A. et al. Ulcerative colitis and autoimmunity induced by loss of myeloid alphav integrins. Proc. Natl. Acad. Sci. USA 104, 15823-15828 (2007).
32. Konkel, J.E. & Chen, W.Balancing acts: the roleofTGF-betainthe mucosal immune system. Trends Mol. Med. 17, 668-676 (2011).
33. Oida, T. & Weiner, H.L. TGF-beta induces surface LAP expression on murine CD4 T cells independent of Foxp3 induction. PLoS One 5, e15523 (2010).
34. Annes, J.P., Chen, Y., Munger, J.S. & Rifkin, D.B. Integrin alphaVbeta6-mediated activation of latent TGF-beta requires the latent TGF-beta binding protein-1. J. Cell. Biol. 165, 723-734 (2004).
35. Clark, D.A., Arck, P.C. & Chaouat, G. Why did your mother reject you? Immunogenetic determinants of the response to environmental selective pressure expressed at the uterine level. Am. J. Reprod. Immunol. 41, 5-22 (1999).
36. Fuss, I.J., Boirivant, M., Lacy, B. & Strober, W.The interrelatedrolesofTGF-beta and IL-10 in the regulation of experimental colitis. J. Immunol. 168, 900-908 (2002).
37. Murai, M. et al. Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat. Immunol. 10, 1178-1184 (2009).
38. Chen, W., Frank, M.E., Jin, W. & Wahl, S.M. TGF-beta released by apoptotic T cells contributes to an immunosuppressive milieu. Immunity 14, 715-725 (2001).
39. Lisboa, F.A. et al. Pregnancy-specific glycoprotein 1 induces endothelial tubulogenesis through interaction with cell surface proteoglycans. J. Biol. Chem. 286, 7577-7586 (2010).
40. Chung, J.S., Shiue, H., Duvic, M., Pandya, A., Cruz, P.D. Jr. & Ariizumi, K. Sezary syndrome cells overexpress syndecan-4 bearing distinct heparan sulfate moieties that suppress T-cell activation by binding DC-HIL and trapping TGF-beta on the cell surface. Blood 117, 3382-3390 (2011).
41. Selick, C.E., Horowitz, G.M., Gratch, M., Scott, R.T. Jr., Navot, D. & Hofmann, G.E. Immunohistochemical localization of transforming growth factor-beta in human implantation sites. J. Clin. Endocrinol. Metab. 78, 592-596 (1994).
42. Keskin, D.B. et al. TGFbeta promotes conversion of CD16+ peripheral blood NK cells into CD16-NK cells with similarities to decidual NK cells. Proc. Natl. Acad. Sci. USA 104, 3378-3383 (2007).
43. Confavreux, C., Hutchinson, M., Hours, M.M., Cortinovis-Tourniaire, P. & Moreau, T. Rate of pregnancy-related relapse in multiple sclerosis. Pregnancy in Multiple Sclerosis Group. N. Engl. J. Med. 339, 285-291 (1998).
44. Beaulieu, D.B. & Kane, S. Inflammatory bowel diseasein pregnancy. World J. Gastroenterol. 17, 22696-22701 (2011).
45. Chen, L. et al. The short isoform of the CEACAM1 receptor in intestinal T cells regulates mucosal immunity and homeostasis via Tfh cell induction. Immunity 37, 930-946 (2012).