Induction and activation of latent transforming growth factor-β1 are carried out by two distinct domains of pregnancy-specific glycoprotein 1 (PSG1)

Journal of Biological Chemistry

Volumn 290, Issue 7, 2015, Pages 4422-4431

  Ballesteros, Angela ^a   Mentink Kane, Margaret M ^b   Warren, James ^b   Kaplan, Gerardo G ^a   Dveksler, Gabriela S ^b  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS;

AMINO ACID SEQUENCE; BIFUNCTIONAL ACTIVITY; N-TERMINAL DOMAINS; TRANSFORMING GROWTH FACTORS;

OBSTETRICS;

GLYCOPROTEIN; LATENCY ASSOCIATED PEPTIDE; LATENT TRANSFORMING GROWTH FACTOR BETA1; PEPTIDES AND PROTEINS; PREGNANCY SPECIFIC GLYCOPROTEIN 1; SMALL LATENT COMPLEX; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; CYTOKINE; MESSENGER RNA; PREGNANCY SPECIFIC BETA1 GLYCOPROTEIN;

A1 DOMAIN; A2 DOMAIN; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; B2 DOMAIN; BINDING AFFINITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENETIC TRANSFECTION; HEK293 CELL LINE; IMMUNOMODULATION; MACROPHAGE CULTURE; MOLECULAR DYNAMICS; MUTAGENESIS; N TERMINAL DOMAIN; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONTENT; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; SURFACE PLASMON RESONANCE; ANIMAL; CELL CULTURE; CYTOLOGY; ENZYME IMMUNOASSAY; FEMALE; GENETICS; HUMAN; MACROPHAGE; METABOLISM; MONOCYTE; MOUSE; PLACENTA; PREGNANCY; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CYTOKINES; FEMALE; HUMANS; IMMUNOENZYME TECHNIQUES; MACROPHAGES; MICE; MONOCYTES; PLACENTA; PREGNANCY; PREGNANCY-SPECIFIC BETA 1-GLYCOPROTEINS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84922787429     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.597518     Document Type: Article

References (39)

1. Teglund, S., Olsen, A., Khan, W. N., Frängsmyr, L., and Hammarström, S. (1994) The pregnancy-specific glycoprotein (PSG) gene cluster on human chromosome 19: fine structure of the 11 PSG genes and identification of 6 new genes forming a third subgroup within the carcinoembryonic antigen (CEA) family. Genomics 23, 669-684
2. McLellan, A. S., Fischer, B., Dveksler, G., Hori, T., Wynne, F., Ball, M., Okumura, K., Moore, T., and Zimmermann, W. (2005) Structure and evolution of the mouse pregnancy-specific glycoprotein (Psg) gene locus. BMC Genomics 6, 4
3. Shanley, D. K., Kiely, P. A., Golla, K., Allen, S., Martin, K., O'Riordan, R. T., Ball, M., Aplin, J. D., Singer, B. B., Caplice, N., Moran, N., and Moore, T. (2013) Pregnancy-specific glycoproteins bind integrin αIIb-β3 and inhibit the platelet-fibrinogen interaction. PLoS ONE 8, e57491
4. Snyder, S. K., Wessner, D. H., Wessells, J. L., Waterhouse, R. M., Wahl, L. M., Zimmermann, W., and Dveksler, G. S. (2001) Pregnancy-specific glycoproteins function as immunomodulators by inducing secretion of IL-10, IL-6 and TGF-β1 by human monocytes. Am. J. Reprod. Immunol. 45, 205-216
5. Martínez, F. F., Knubel, C. P., Sánchez, M. C., Cervi, L., and Motrán, C. C. (2012) Pregnancy-specific glycoprotein 1a activates dendritic cells to provide signals for Th17-, Th2-, and Treg-cell polarization. Eur. J. Immunol. 42, 1573-1584
6. Motrán, C. C., Díaz, F. L., Gruppi, A., Slavin, D., Chatton, B., and Bocco, J. L. (2002) Human pregnancy-specific glycoprotein 1a (PSG1a) induces alternative activation in human and mouse monocytes and suppresses the accessory cell-dependent T cell proliferation. J. Leukoc. Biol. 72, 512-521
7. Pihl, K., Larsen, T., Laursen, I., Krebs, L., and Christiansen, M. (2009) First trimester maternal serum pregnancy-specific b-1-glycoprotein (SP1) as a marker of adverse pregnancy outcome. Prenat. Diagn. 29, 1256-1261
8. Waterhouse, R., Ha, C., and Dveksler, G. S. (2002) Murine CD9 is the receptor for pregnancy-specific glycoprotein 17. J. Exp. Med. 195, 277-282
9. Sulkowski, G. N., Warren, J., Ha, C. T., and Dveksler, G. S. (2011) Characterization of receptors for murine pregnancy specific glycoproteins 17 and 23. Placenta 32, 603-610
10. Lisboa, F. A., Warren, J., Sulkowski, G., Aparicio, M., David, G., Zudaire, E., and Dveksler, G. S. (2011) Pregnancy-specific glycoprotein 1 induces endothelial tubulogenesis through interaction with cell surface proteoglycans. J. Biol. Chem. 286, 7577-7586
11. Li, M. O., Wan, Y. Y., Sanjabi, S., Robertson, A. K., and Flavell, R. A. (2006) Transforming growth factor-β regulation of immune responses. Annu. Rev. Immunol. 24, 99-146
12. Annes, J. P., Munger, J. S., and Rifkin, D. B. (2003) Making sense of latent TGF-β activation. J. Cell Sci. 116, 217-224
13. Glinka, Y., and Prud'homme, G. J. (2008) Neuropilin-1 is a receptor for transforming growth factor β-1, activates its latent form, and promotes regulatory T cell activity. J. Leukoc. Biol. 84, 302-310
14. Ohno, M., Cooke, J. P., Dzau, V. J., and Gibbons, G. H. (1995) Fluid shear stress induces endothelial transforming growth factor β-1 transcription and production. Modulation by potassium channel blockade. J. Clin. Invest. 95, 1363-1369
15. Blois, S. M., Sulkowski, G., Tirado-González, I., Warren, J., Freitag, N., Klapp, B. F., Rifkin, D., Fuss, I., Strober, W., and Dveksler, G. S. (2014) Pregnancy-specific glycoprotein 1 (PSG1) activates TGF-β and prevents dextran sodium sulfate (DSS)-induced colitis in mice. Mucosal Immunol. 7, 348-358
16. Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y., and Henson, P. M. (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/ paracrine mechanisms involving TGF-β, PGE2, and PAF. J. Clin. Invest. 101, 890-898
17. Xiong, W., Frasch, S. C., Thomas, S. M., Bratton, D. L., and Henson, P. M. (2013) Induction of TGF-β1 synthesis by macrophages in response to apoptotic cells requires activation of the scavenger receptor CD36. PLoS ONE 8, e72772
18. Toossi, Z., Young, T. G., Averill, L. E., Hamilton, B. D., Shiratsuchi, H., and Ellner, J. J. (1995) Induction of transforming growth factorβ1 by purified protein derivative of Mycobacterium tuberculosis. Infect. Immun. 63, 224-228
19. Toossi, Z., Hirsch, C. S., Hamilton, B. D., Knuth, C. K., Friedlander, M. A., and Rich, E. A. (1996) Decreased production of TGF-β1 by human alveolar macrophages compared with blood monocytes. J. Immunol. 156, 3461-3468
20. Abe, M., Harpel, J. G., Metz, C. N., Nunes, I., Loskutoff, D. J., and Rifkin, D. B. (1994) An assay for transforming growth factor-β using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal. Biochem. 216, 276-284
21. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISSMODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201
22. Guex, N., Peitsch, M. C., and Schwede, T. (2009) Automated comparative protein structure modeling with SWISS-MODEL and Swiss-PdbViewer: a historical perspective. Electrophoresis 30, S162-S173
23. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
24. Bhattacharya, D., and Cheng, J. (2013) 3Drefine: consistent protein structure refinement by optimizing hydrogen bonding network and atomiclevel energy minimization. Proteins 81, 119-131
25. Annes, J. P., Chen, Y., Munger, J. S., and Rifkin, D. B. (2004) IntegrinαVβ6-mediated activation of latent TGF-β requires the latent TGF-β binding protein-1. J. Cell Biol. 165, 723-734
26. Ribeiro, S. M., Poczatek, M., Schultz-Cherry, S., Villain, M., and MurphyUllrich, J. E. (1999) The activation sequence of thrombospondin-1 interacts with the latency-associated peptide to regulate activation of latent transforming growth factor-β. J. Biol. Chem. 274, 13586-13593
27. Osborne, J. C., Jr., Rosen, S. W., Nilsson, B., Calvert, I., and Bohn, H. (1982) Physicochemical studies of pregnancy-specific β1-glycoprotein: unusual ultracentrifugal and circular dichroic properties. Biochemistry 21, 5523-5528
28. Alcaraz, L. B., Exposito, J. Y., Chuvin, N., Pommier, R. M., Cluzel, C., Martel, S., Sentis, S., Bartholin, L., Lethias, C., and Valcourt, U. (2014) Tenascin-X promotes epithelial-to-mesenchymal transition by activating latent TGF-β. J. Cell Biol. 205, 409-428
29. Zhou, G. Q., and Hammarström, S. (2001) Pregnancy-specific glycoprotein (PSG) in baboon (Papio hamadryas): family size, domain structure, and prediction of a functional region in primate PSGs. Biol. Reprod. 64, 90-99
30. Lee, J. N., Grudzinskas, J. G., and Chard, T. (1979) Circulating levels of pregnancy proteins in early and late pregnancy in relation to placental tissue concentration. Br. J. Obstet. Gynaecol. 86, 888-890
31. Zhou, G. Q., Baranov, V., Zimmermann, W., Grunert, F., Erhard, B., Mincheva-Nilsson, L., Hammarström, S., and Thompson, J. (1997) Highly specific monoclonal antibody demonstrates that pregnancy-specific glycoprotein (PSG) is limited to syncytiotrophoblast in human early and term placenta. Placenta 18, 491-501
32. Tangerås, L. H., Stødle, G. S., Olsen, G. D., Leknes, A. H., Gundersen, A. S., Skei, B., Vikdal, A. J., Ryan, L., Steinkjer, B., Myklebost, M. F., Langaas, M., Austgulen, R., and Iversen, A. C. (2014) Functional Toll-like receptors in primary first-trimester trophoblasts. J. Reprod. Immunol. 106, 88-99
33. Fardini, Y., Chung, P., Dumm, R., Joshi, N., and Han, Y. W. (2010) Transmission of diverse oral bacteria to murine placenta: evidence for the oral microbiome as a potential source of intrauterine infection. Infect. Immun. 78, 1789-1796
34. Aagaard, K., Ma, J., Antony, K. M., Ganu, R., Petrosino, J., and Versalovic, J. (2014) The placenta harbors a unique microbiome. Sci. Transl. Med. 6, 237ra265
35. Radaev, S., Zou, Z., Huang, T., Lafer, E. M., Hinck, A. P., and Sun, P. D. (2010) Ternary complex of transforming growth factor-β1 reveals isoform- specific ligand recognition and receptor recruitment in the superfamily. J. Biol. Chem. 285, 14806-14814
36. Bailly, S., Brand, C., Chambaz, E. M., and Feige, J. J. (1997) Analysis of small latent transforming growth factor-β complex formation and dissociation by surface plasmon resonance. Absence of direct interaction with thrombospondins. J. Biol. Chem. 272, 16329-16334
37. Shi, M., Zhu, J., Wang, R., Chen, X., Mi, L., Walz, T., and Springer, T. A. (2011) Latent TGF-β structure and activation. Nature 474, 343-349
38. Gray-Owen, S. D., and Blumberg, R. S. (2006) CEACAM1: contact-dependent control of immunity. Nat. Rev. Immunol. 6, 433-446
39. Dveksler, G. S., Dieffenbach, C. W., Cardellichio, C. B., McCuaig, K., Pensiero, M. N., Jiang, G. S., Beauchemin, N., and Holmes, K. V. (1993) Several members of the mouse carcinoembryonic antigen-related glycoprotein family are functional receptors for the coronavirus mouse hepatitis virus- A59. J. Virol. 67, 1-8