Glycosylation oftwisted gastrulation is required for BMP binding and activity during craniofacial development

Frontiers in Physiology

Volumn 2 SEP, Issue , 2011, Pages

  Billington Jr , Charles J ^a,b   Fiebig, Juliane E ^c   Forsman, Cynthia L ^a,b   Pham, Lan ^b   Burbach, Nathan ^a   Sun, Mu ^d   Jaskoll, Tina ^e   Mansky, Kim ^b   Gopalakrishnan, Rajaram ^b   O'Connor, Michael B ^b   Mueller, Thomas D ^c   Petryk, Anna ^a,b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d GLAXOSMITHKLINE   (China)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

BMP; Glycosylation; Mandibular explants; Msx2; Surface plasmon resonance analysis; Twisted gastrulation

Indexed keywords

EID: 84866180783     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2011.00059     Document Type: Article

References (50)

1. Avsian-Kretchmer, O., and Hsueh, A. J. (2004). Comparative genomic analysis of the eight-membered ring cystine knot-containing bone mor-phogenetic protein antagonists. Mol. Endocrinol. 18,1-12.
2. Barbosa, J. A., Santos-Aguado, J., Mentzer, S. J., Strominger, J. L., Burakoff, S. J., and Biro, P. A. (1987). Site-directed mutagenesis of class I HLA genes. Role of glycosyla-tion in surface expression and functional recognition. J. Exp. Med. 166, 1329-1350.
3. Benz, I., and Schmidt, M. A. (2001). Glycosylation with heptose residues mediated by the aah gene product is essential for adherence of the AIDA-I adhesin. Mol. Microbiol. 40, 1403-1413.
4. Bier, E. (2008). Intriguing extracellular regulation of BMP signaling. Dev. Cell 15, 176-177.
5. Billington, C. J.Jr , Ng, B., Forsman, C., Schmidt, B., Bagchi, A., Symer, D. E., Schotta, G., Gopalakrishnan, R., Sarver, A. L., and Petryk, A. (2011). The molecular and cellular basis of variable craniofacial phenotypes and their genetic rescue in Twisted gas-trulation mutant mice. Dev. Biol. 355,21-31.
6. Blitz, I. L., Cho, K. W., and Chang, C. (2003). Twisted gastrulation loss-of-function analyses support its role as a BMP inhibitor during early Xenopus embryogenesis. Development 130, 4975-4988.
7. Buller, A. L., Hastings, G. A., Kirkness, E. F., and Fraser, C. M. (1994). Site-directed mutagenesis of N-linked glycosylation sites on the gamma-aminobutyric acid type A receptor alpha 1 subunit. Mol. Pharmacol. 46, 858-865.
8. Caragea, C., Sinapov, J., Silvescu, A., Dobbs, D., and Honavar, V. (2007). Glycosylation site prediction using ensembles of support vector machine classifiers. BMC Bioinfor-matics 8, 438. doi: 10.1186/1471-2105-8-438
9. Chang, C., Holtzman, D. A., Chau, S., Chickering, T., Woolf, E. A., Holmgren, L. M., Bodorova, J., Gearing, D. P., Holmes, W. E., and Brivanlou, A. H. (2001). Twisted gastrulation can function as a BMP antagonist. Nature 410, 483-487.
10. Ekanayake, S., and Hall, B. K. (1997). The in vivo and in vitro effects of bone morphogenetic protein-2 on the development of the chick mandible. Int. J. Dev. Biol. 41,67-81.
11. Gavel, Y., and Von Heijne, G. (1990). Sequence differences between glyco-sylatedandnon-glycosylatedAsn-X-Thr/Ser acceptor sites: implications for protein engineering. Protein Eng. 3, 433-442.
12. Gazzerro, E., Deregowski, V., Stadmeyer, L., Gale, N. W., Economides, A. N., and Canalis, E. (2006). Twisted gastrulation, a bone morphogenetic protein agonist/antagonist, is not required for post-natal skeletal function. Bone 39, 1252-1260.
13. Groppe, J., Greenwald, J., Wiater, E., Rodriguez-Leon, J., Economides, A. N., Kwiatkowski, W., Affolter, M., Vale, W. W., Belmonte, J. C., and Choe, S. (2002). Structural basis of BMP signalling inhibition by the cystine knot protein Noggin. Nature 420,636-642.
14. Gumienny, T. L., and Padgett, R. W. (2002). The other side of TGF-beta superfamily signal regulation: thinking outside the cell. Trends Endocrinol. Metab. 13, 295-299.
15. Heinecke, K., Seher, A., Schmitz, W., Mueller, T. D., Sebald, W., and Nickel, J. (2009). Receptor oligomerization and beyond: a case study in bone morphogenetic proteins. BMC Biol. 7, 59. doi: 10.1186/1741-7007-7-59
16. Henderson, G. E., Isett, K. D., and Gerngross, T. U. (2011). Site-specific modification of recombinant proteins: a novel platform for modifying glycoproteins expressed in E. coli. Bioconjug. Chem. 22, 903-912.
17. Jarvis, D. L., Kawar, Z. S., and Hol-lister, J. R. (1998). Engineering N-glycosylation pathways in the baculovirus-insect cell system. Curr. Opin. Biotechnol. 9, 528-533.
18. Jaskoll, T., Abichaker, G., Witcher, D., Sala, E G., Bellusci, S., Hajihos-seini, M. K., and Melnick, M. (2005). FGF10/FGFR2b signaling plays essential roles during in vivo embryonic submandibular salivary gland morphogenesis. BMC Dev. Biol. 5, 11. doi: 10.1186/1471-213X-5-11
19. Kamimura, M., Matsumoto, K., Koshiba-Takeuchi, K., and Ogura, T. (2004). Vertebrate crossveinless 2 is secreted and acts as an extracellular modulator of the BMP signaling cascade. Dev. Dyn. 230, 434-445.
20. Larrain, J., Oelgeschlager, M., Ketpura, N. I., Reversade, B., Zakin, L., and De Robertis, E. M. (2001). Prote-olytic cleavage of chordin as a switch for the dual activities of Twisted gastrulation in BMP signaling. Development 128,4439-4447.
21. Lindenthal, C., and Elsinghorst, E. A. (1999). Identification of a glyco-protein produced by enterotoxigenic Escherichia coli. Infect. Immun. 67, 4084-4091.
22. Mackenzie, A., Ferguson, M. W., and Sharpe, P. T. (1992). Expression patterns of the homeobox gene, Hox-8, in the mouse embryo suggest a role in specifying tooth initiation and shape. Development 115, 403-420.
23. Mackenzie, B., Wolff, R., Lowe, N., Billington, C. J., Peterson, A., Schmidt, B., Graf, D., Mina, M., Gopalakrishnan, R., and Petryk, A. (2009). Twisted gastrulation limits apoptosis in the distal region of the mandibular arch in mice. Dev. Biol. 328, 13-23.
24. Mason, E. D., Konrad, K. D., Webb, C. D., and Marsh, J. L. (1994). Dorsal midline fate in Drosophila embryos requires Twisted gastrulation, a gene encoding a secreted protein related to human connective tissue growth factor. Genes Dev. 8, 1489-1501.
25. Melnick, M., Witcher, D., Bringas, P. Jr., Carlsson, P., and Jaskoll, T. (2005). Meckel's cartilage differentiation is dependent on hedgehog signaling. Cells Tissues Organs 179,146-157.
26. Mina, M., Wang, Y. H., Ivanisevic, A. M., Upholt, W B., and Rodgers, B. (2002). Region- and stage-specific effects of FGFs and BMPs in chick mandibular morphogenesis. Dev. Dyn. 223, 333-352.
27. Neuberger, A., and Marshall, R. D. (1968). "Aspects of the structure of glycoproteins," in Symposium on Foods - Carbohydrates and their Roles, eds H. W Schultz, R. F. Cain, and R. W. Wrolstad (Westport, CT: Avi Publishing Co.), 115-132.
28. Nosaka, T., Morita, S., Kitamura, H., Nakajima, H., Shibata, F., Morikawa, Y., Kataoka, Y., Ebihara, Y., Kawashima, T., Itoh, T., Ozaki, K., Senba, E., Tsuji, K., Makishima, F., Yoshida,N.,andKitamura,T. (2003). Mammalian Twisted gastrulation is essential for skeleto-lymphogenesis. Mol. Cell. Biol. 23, 2969-2980.
29. Oelgeschlager, M., Larrain, J., Geissert, D., and De Robertis, E. M. (2000). The evolutionarily conserved BMP-binding protein Twisted gastrulation promotes BMP signalling. Nature 405, 757-763.
30. Oelgeschlager, M., Reversade, B., Larrain, J., Little, S., Mullins, M. C., and De Robertis, E. M. (2003). The pro-BMP activity of Twisted gastrulation is independent of BMP binding. Development 130,4047-4056.
31. Oelgeschlager, M., Tran, U., Grubisic, K., and De Robertis, E. M. (2004). Identification of a second Xenopus Twisted gastrulation gene. Int. J. Dev. Biol. 48, 57-61.
32. Petryk, A., Anderson, R., Jarcho, M. P., Leaf, H., Carlson, C. S., Klin-gensmith, J., Shawlot, W., and O'connor, M. B. (2004). The mammalian Twisted gastrulation gene functions in foregut and craniofa-cial development. Dev. Biol. 267, 374-386.
33. Ross,J. J.,Shimmi, O.,Vilmos, P., Petryk, A., Kim, H., Gaudenz, K., Herman-son, S., Ekker, S. C., O'connor, M. B., and Marsh, J. L. (2001). Twisted gastrulation is a conserved extracellular BMP antagonist. Nature 410, 479-483.
34. Ruppert, R., Hoffmann, E., and Sebald, W. (1996). Human bone morpho-genetic protein 2 contains a heparin-binding site which modifies its biological activity. Eur. J. Biochem. 237, 295-302.
35. Saremba, S., Nickel, J., Seher, A., Kotzsch, A., Sebald, W., and Mueller, T. D. (2008). Type I receptor binding of bone morphogenetic protein 6 is dependent on N-glycosylation of the ligand.FEBS J. 275, 172-183.
36. Sasaki,H.,andHogan,B.L. (1993). Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118,47-59.
37. Scott, I. C., Blitz, I. L., Pappano, W. N., Maas, S. A., Cho, K. W., and Greenspan, D. S. (2001). Homo-logues of Twisted gastrulation are extracellular cofactors in antagonism of BMP signalling. Nature 410, 475-478.
38. Semba, I., Nonaka, K., Takahashi, I., Takahashi, K., Dashner, R., Shum, L., Nuckolls, G. H., and Slavkin, H. C. (2000). Positionally-dependent chondrogenesis induced by BMP4 is co-regulated bySox9 andMsx2. Dev. Dyn. 217, 401-414.
39. Spiro, R. G. (2002). Protein glycosyla-tion: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 12, 43R-56R.
40. Stanley, E., Biben, C., Kotecha, S., Fabri, L., Tajbakhsh, S., Wang, C. C., Hatzistavrou, T., Roberts, B., Drinkwater, C., Lah, M., Buckingham, M., Hilton, D., Nash, A., Mohun, T., and Harvey, R. P. (1998). DAN is a secreted glycoprotein related to Xenopus cerberus. Mech. Dev. 77, 173-184.
41. Tomiya, N., Narang, S., Lee, Y. C., and Betenbaugh, M. J. (2004). Comparing N-glycan processing in mammalian cell lines to native and engineered lepidopteran insect cell lines. Glycoconj. J. 21, 343-360.
42. Tucker, A. S., Matthews, K. L., and Sharpe, P. T. (1998). Transformation of tooth type induced by inhibition of BMP signaling. Science 282, 1136-1138.
43. Vilmos, P., Gaudenz, K., Hegedus, Z., and Marsh, J. L. (2001). The Twisted gastrulation family of proteins, together with the IGFBP and CCN families, comprise the TIC superfamily of cysteine rich secreted factors. Mol. Pathol. 54, 317-323.
44. Wacker, M., Linton, D., Hitchen, P. G., Nita-Lazar, M., Haslam, S. M., North, S. J., Panico, M., Morris, H. R., Dell, A., Wren, B. W., and Aebi, M. (2002). N-linked glycosylationin Campylobacter jejuni and its functional transfer into E. coli. Science 298,1790-1793.
45. Walsh, G., and Jefferis, R. (2006). Post-translational modifications in the context of therapeutic proteins. Nat. Biotechnol. 24, 1241-1252.
46. Westmoreland, J. J., Takahashi, S., and Wright, C. V. (2007). Xenopus lefty requires proprotein cleavage but not N-linked glycosylation to inhibit nodal signaling. Dev. Dyn. 236, 2050-2061.
47. Wu, Y. I., Munshi, H. G., Sen, R., Sni-pas, S. J., Salvesen, G. S., Fridman, R., and Stack, M. S. (2004). Glycosylation broadens the substrate profile of membrane type 1 matrix metalloproteinase. J. Biol. Chem. 279, 8278-8289.
48. Yamaguchi, K., Akai, K., Kawanishi, G., Ueda, M., Masuda, S., and Sasaki, R. (1991). Effects of site-directed removal of N-glycosylation sites in human erythropoietin on its production and biological properties. J. Biol. Chem. 266, 20434-20439.
49. Zakin, L., and De Robertis, E. M. (2004). Inactivation of mouse Twisted gastrulation reveals its role in promoting Bmp4 activity during fore-brain development. Development 131,413-424.
50. Zakin, L., Reversade, B., Kuroda, H., Lyons, K. M., and De Robertis, E. M. (2005). Sirenomelia in Bmp7 and Tsg compound mutant mice: requirement for Bmp signaling in the development of ventral posterior mesoderm. Development 132, 2489-2499.