A core domain of the BMP2 proregion is sufficient for the biogenesis of mature homodimeric growth factor

Biological Chemistry

Volumn 396, Issue 3, 2015, Pages 215-223

  Kuhfahl, Silke ^a   Schwarz, Elisabeth ^a  

^a MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

bone morphogenetic protein; complementation; intramolecular chaperone; proregion; subdomain

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; GLUCAN SYNTHASE; GROWTH DIFFERENTIATION FACTOR 5; GROWTH FACTOR; RECOMBINANT PROTEIN;

ARTICLE; BIOGENESIS; CELL CULTURE; COVALENT BOND; ENZYME LINKED IMMUNOSORBENT ASSAY; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN SECRETION; AMINO ACID SEQUENCE; BIOPHYSICS; BIOSYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; HEK293 CELL LINE; HUMAN; MOLECULAR GENETICS; MOLECULAR WEIGHT; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; STRUCTURAL HOMOLOGY; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; BIOPHYSICAL PHENOMENA; BONE MORPHOGENETIC PROTEIN 2; HEK293 CELLS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; STRUCTURAL HOMOLOGY, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84922553433     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2014-0220     Document Type: Article

References (40)

1. Bailly, S., Brand, C., Chambaz, E.M., and Feige, J.J. (1997). Analysis of small latent transforming growth factor-complex formation and dissociation by surface plasmon resonance. Absence of direct interaction with thrombospondins. J. Biol. Chem. 272, 16329-16334.
2. Bonewald, L.F., Wakefield, L., Oreffo, R.O., Escobedo, A., Twardzik, D.R., and Mundy, G.R. (1991). Latent forms of transforming growth factor-(TGF) derived from bone cultures: identification of a naturally occurring 100-kDa complex with similarity to recombinant latent TGF?. Mol. Endocrinol. 5, 741-751.
3. Boettinger, E.P., Factor, V.M., Tsang, M.L., Weatherbee, J.A., Kopp, J.B., Qian, S.W., Wakefield, L.M., Roberts, A.B., Thorgeirsson, S.S., and Sporn, M.B. (1996). The recombinant proregion of transforming growth factor 1 (latency-associated peptide) inhibits active transforming growth factor 1 in transgenic mice. Proc. Natl. Acad. Sci. USA 93, 5877-5882.
4. Brunner, A.M., Marquardt, H., Malacko, A.R., Lioubin, M.N., and Purchio, A.F. (1989). Site-directed mutagenesis of cysteine residues in the pro region of the transforming growth factor 1 precursor. Expression and characterization of mutant proteins. J. Biol. Chem. 264, 13660-13664.
5. Constam, D.B. and Robertson, E.J. (1999). Regulation of bone morphogenetic protein activity by pro domains and proprotein convertases. J. Cell Biol. 144, 139-149.
6. Cui, Y., Hackenmiller, R., Berg, L., Jean, F., Nakayama, T., Thomas, G., and Christian, J.L. (2001). The activity and signaling range of mature BMP-4 is regulated by sequential cleavage at two sites within the prodomain of the precursor. Genes Dev. 15, 2797-2802.
7. Eswar, N., John, B., Mirkovic, N., Fiser, A., Ilyin, V.A., Pieper, U., Stuart, A.C., Marti-Renom, M.A., Madhusudhan, M.S., Yerkovich, B., et al. (2003). Tools for comparative protein structure modeling and analysis. Nucleic Acids Res. 31, 3375-3380.
8. Fu, X., Inouye, M., and Shinde, U. (2000). Folding pathway mediated by an intramolecular chaperone. The inhibitory and chaperone functions of the subtilisin propeptide are not obligatorily linked. J. Biol. Chem. 275, 16871-16878.
9. Gentry, L.E. and Nash, B.W. (1990). The pro domain of pre-protransforming growth factor 1 when independently expressed is a functional binding protein for the mature growth factor. Biochemistry. 29, 6851-6857.
10. Gray, A.M. and Mason, A.J. (1990). Requirement for activin A and transforming growth factor 1 pro-regions in homodimer assembly. Science 247, 1328-1330.
11. Gregory, K.E., Ono, R.N., Charbonneau, N.L., Kuo, C.L., Keene, D.R., Bachinger, H.P., and Sakai, L.Y. (2005). The prodomain of BMP-7 targets the BMP-7 complex to the extracellular matrix. J. Biol. Chem. 280, 27970-27980.
12. Hammonds, R.G., Jr., Schwall, R., Dudley, A., Berkemeier, L., Lai, C., Lee, J., Cunningham, N., Reddi, A.H., Wood, W.I., and Mason, A.J. (1991). Bone-inducing activity of mature BMP-2b produced from a hybrid BMP-2a/2b precursor. Mol. Endocrinol. 5, 149-155.
13. Hauburger, A., von Einem, S., Schwaerzer, G.K., Buttstedt, A., Zebisch, M., Schraml, M., Hortschansky, P., Knaus, P., and Schwarz, E. (2009). The pro-form of BMP-2 interferes with BMP-2 signalling by competing with BMP-2 for IA receptor binding. FEBS J. 276, 6386-6398.
14. Hillger, F., Herr, G., Rudolph, R., and Schwarz, E. (2005). Biophysical comparison of BMP-2, ProBMP-2, and the free pro-peptide reveals stabilization of the pro-peptide by the mature growth factor. J. Biol. Chem. 280, 14974-14980.
15. Israel, D.I., Nove, J., Kerns, K.M., Moutsatsos, I.K., and Kaufman, R.J. (1992). Expression and characterization of bone morphogenetic protein-2 in Chinese hamster ovary cells. Growth Factors. 7, 139-150.
16. Janssens, K., Vanhoenacker, F., Bonduelle, M., Verbruggen, L., Van Maldergem, L., Ralston, S., Guanabens, N., Migone, N., Wientroub, S., Divizia, M.T., et al. (2006). Camurati-Engelmann disease: review of the clinical, radiological, and molecular data of 24 families and implications for diagnosis and treatment. J. Med. Genet. 43, 1-11.
17. Jones, W.K., Richmond, E.A., White, K., Sasak, H., Kusmik, W., Smart, J., Oppermann, H., Rueger, D.C., and Tucker, R.F. (1994). Osteogenic protein-1 (OP-1) expression and processing in Chinese hamster ovary cells: isolation of a soluble complex containing the mature and pro-domains of OP-1. Growth Factors 11, 215-225.
18. Kliemannel, M., Rattenholl, A., Golbik, R., Balbach, J., Lilie, H., Rudolph, R., and Schwarz, E. (2004). The mature part of proNGF induces the structure of its pro-peptide. FEBS Lett. 566, 207-212.
19. Kuhfahl, S., Hauburger, A., Thieme, T., Groppe, J., Ihling, C., Tomic, S., Schutkowski, M., Sinz, A., and Schwarz, E. (2011). Identification of a core domain within the proregion of bone morphogenetic proteins that interacts with the dimeric, mature domain. Biochem. Biophys. Res. Commun. 408, 300-305.
20. Lee, S.J. and McPherron, A.C. (2001). Regulation of myostatin activity and muscle growth. Proc. Natl. Acad. Sci. USA 98, 9306-9311.
21. McDonald, N.Q. and Hendrickson, W.A. (1993). A structural superfamily of growth factors containing a cystine knot motif. Cell 73, 421-424.
22. Miller, D.M., Ogawa, Y., Iwata, K.K., ten Dijke, P., Purchio, A.F., Soloff, M.S., and Gentry, L.E. (1992). Characterization of the binding of transforming growth factor-1,-2, and-3 to recombinant 1-latency-associated peptide. Mol. Endocrinol. 6, 694-702.
23. Miyazono, K., Hellman, U., Wernstedt, C., and Heldin, C.H. (1988). Latent high molecular weight complex of transforming growth factor 1. Purification from human platelets and structural characterization. J. Biol. Chem. 263, 6407-6415.
24. Mueller, T.D. and Nickel, J. (2012). Promiscuity and specificity in BMP receptor activation. FEBS Lett. 586, 1846-1859.
25. Pace, C.N. and Shaw, K.L. (2000). Linear extrapolation method of analyzing solvent denaturation curves. Proteins (Suppl.) 4, 1-7.
26. Peters, R.J., Shiau, A.K., Sohl, J.L., Anderson, D.E., Tang, G., Silen, J.L., and Agard, D.A. (1998). Pro region C-terminus:protease active site interactions are critical in catalyzing the folding of -lytic protease. Biochemistry 37, 12058-12067.
27. Ploeger, F., Seemann, P., Schmidt-von Kegler, M., Lehmann, K., Seidel, J., Kjaer, K.W., Pohl, J., and Mundlos, S. (2008). Brachydactyly type A2 associated with a defect in proGDF5 processing. Hum. Mol. Genet. 17, 1222-1233.
28. Roedel, E.K., Schwarz, E., and Kanse, S.M. (2013). The factor VII-activating protease (FSAP) enhances the activity of bone morphogenetic protein-2 (BMP-2). J. Biol. Chem. 288, 7193-7203.
29. Santoro, M.M. and Bolen, D.W. (1988). Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl -chymotrypsin using different denaturants. Biochemistry 27, 8063-8068.
30. Scheufler, C., Sebald, W., and Hulsmeyer, M. (1999). Crystal structure of human bone morphogenetic protein-2 at 2.7 Å resolution. J. Mol. Biol. 287, 103-115.
31. Shi, M., Zhu, J., Wang, R., Chen, X., Mi, L., Walz, T., and Springer, T.A. (2011). Latent TGF-structure and activation. Nature 474, 343-349.
32. Sopory, S., Nelsen, S.M., Degnin, C., Wong, C., and Christian, J.L. (2006). Regulation of bone morphogenetic protein-4 activity by sequence elements within the prodomain. J. Biol. Chem. 281, 34021-34031.
33. Vitt, U.A., Hsu, S.Y., and Hsueh, A.J. (2001). Evolution and classification of cystine knot-containing hormones and related extracellular signaling molecules. Mol. Endocrinol. 15, 681-694.
34. von Einem, S., Erler, S., Bigl, K., Frerich, B., and Schwarz, E. (2011). The pro-form of BMP-2 exhibits a delayed and reduced activity when compared to mature BMP-2. Growth Factors 29, 63-71.
35. Wakefield, L.M., Smith, D.M., Flanders, K.C., and Sporn, M.B. (1988). Latent transforming growth factor-from human platelets. A high molecular weight complex containing precursor sequences. J. Biol. Chem. 263, 7646-7654.
36. Walton, K.L., Makanji, Y., Chen, J., Wilce, M.C., Chan, K.L., Robertson, D.M., and Harrison, C.A. (2010). Two distinct regions of latency-associated peptide coordinate stability of the latent transforming growth factor-1 complex. J. Biol. Chem. 285, 17029-17037.
37. Wang, E.A., Rosen, V., D'Alessandro, J.S., Bauduy, M., Cordes, P., Harada, T., Israel, D.I., Hewick, R.M., Kerns, K.M., LaPan, P., et al. (1990). Recombinant human bone morphogenetic protein induces bone formation. Proc. Natl. Acad. Sci. USA 87, 2220-2224.
38. Wu, M.Y. and Hill, C.S. (2009). TGF-superfamily signaling in embryonic development and homeostasis. Dev Cell. 16, 329-343.
39. Yang, Z., Mu, Z., Dabovic, B., Jurukovski, V., Yu, D., Sung, J., Xiong, X., and Munger, J.S. (2007). Absence of integrin-mediated TGF1 activation in vivo recapitulates the phenotype of TGF1-null mice. J. Cell Biol. 176, 787-793.
40. Yang, W., Cao, L., Liu, W., Jiang, L., Sun, M., Zhang, D., Wang, S., Lo, W.H., Luo, Y., and Zhang, X. (2008). Novel point mutations in GDF5 associated with two distinct limb malformations in Chinese: brachydactyly type C and proximal symphalangism. J. Hum. Genet. 53, 368-374.