BMP-4 is proteolytically activated by furin and/or PC6 during vertebrate embryonic development

EMBO Journal

Volumn 17, Issue 16, 1998, Pages 4735-4743

  Cui, Yanzhen ^a   Jean, François ^a   Thomas, Gary ^a   Christian, Jan L ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

1 antitrypsin Portland; BMP 4; Furin; Proprotein convertase; Xenopus

Indexed keywords

ALPHA 1 ANTITRYPSIN; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 4; ENZYME INHIBITOR; FURIN; PROPROTEIN CONVERTASE; PROTEINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; MESODERM; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN SYNTHESIS; RECEPTOR BINDING; RNA TRANSLATION; SIGNAL TRANSDUCTION; XENOPUS;

ALPHA 1-ANTITRYPSIN; ANIMALS; BASE SEQUENCE; BONE MORPHOGENETIC PROTEINS; CELL LINEAGE; DNA PRIMERS; ECTODERM; EMBRYO, NONMAMMALIAN; FURIN; HYDROLYSIS; MESODERM; PROPROTEIN CONVERTASE 5; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; SUBTILISINS; XENOPUS;

ANIMALIA; VERTEBRATA;

EID: 0032541405     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.16.4735     Document Type: Article

References (52)

1. Anderson,E.D., VanSlyke,J.K., Thulin,C.D. Jean,F. and Thomas,G. (1997) Activation of the furin endoprotease is a multiple-step process: requirements for acidification and internal propeptide cleavage. EMBO J., 16, 1508-1518.
2. Aono,A., Hazama,M., Notoya,K., Taketomi,S., Yamasaki,H., Tsukuda,R., Sasaki,S. and Fujisawa,Y. (1995) Potent ectopic bone-inducing activity of bone morphogenetic protein-4/7 heterodimer. Biochem. Biophys. Res. Commun., 210, 670-677.
3. Bolce,M.E., Hemmati-Brivanlou,A., Kushner,P.D. and Harland,R.M. (1992) Ventral ectoderm of Xenopus forms neural tissues, including hindbrain, in response to activin. Development, 115, 681-688.
4. Breslin,M.B., Lindberg,I., Benjannet,S., Mathis,J.P., Lazure,C. and Seidah,N. (1993) Differential processing of proenkephalin by prohormone convertases 1 (3) and 2 and furin. J. Biol. Client., 268, 27084-27093.
5. Bresnahan,P.A., Hayflick,J.S., Molloy,S.S. and Thomas,G. (1993) Endoproteolysis of growth factors and other nonendocrine precursor proteins. In Loh,Y.P. (ed.) Mechanisms of Intracellular Trafficking and Processing of Proproteins. CRC Press, Boca Raton, FL, pp. 225-250.
6. Candia,A.F., Watabe,T., Hawley,S.H.B., Onichtchouk,D., Zhang,Y., Derynck,R., Niehrs,C. and Cho,K.W.Y. (1997) Cellular interpretation of multiple TGF-β signals: intracellular antagonism between activin/ BVg1 and BMP-2/4 signaling mediated by Smads. Development, 124, 4467-4480.
7. Cho,K.W.Y. Blumberg,B., Steinbesser,H. and DeRobertis,E.M. (1991) Molecular nature of the organizer: the role of the Xenopus homeobox gene goosecoid. Cell, 67, 1111-1120.
8. Christian,J.L., McMahon,J.A., McMahon,A.P. and Moon,R.T. (1991) Xwnt-8, a Xenopus Wnt-1/int-1-related gene responsive to mesoderm inducing factors, may play a role in ventral mesodermal patterning during embryogenesis. Development, 111, 1045-1056.
9. Constam,D.B., Calfon,M. and Robertson,E.J. (1996) SPC4, SPC6 and the novel protease SPC7 are coexpressed with bone morphogenetic proteins at distinct sties during embryogenesis. J. Cell Biol., 134, 181-191.
10. Creemers,J.W.M., Siezen,R.J., Roebroek,A.J.M., Ayoubi,T.A.Y., Huylebroeck,D. and Van de Ven,W.J.M. (1993) Modulation of furinmediated proprotein processing activity by site directed mutagenesis. J. Biol. Chem., 268, 21826-21834.
11. Cui,Y., Tian,Q. and Christian,J.L. (1996) Synergistic effects of Vg1 and Wnt signals in the specification of dorsal mesoderm and endoderm. Dev. Biol., 180, 22-34.
12. Dubois,C.M., Laprise,M.H., Blanchetter,F., Gentry,L.E. and LeDuc,R. (1995) Processing of transforming growth factor beta 1 precursor by human furin convertase. J. Biol. Chem., 270, 10618-10624.
13. Fainsod,A., Steinbesser,H. and DeRobertis,E. (1994) On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo. EMBO J., 13, 5015-5025.
14. Graff,J.M. (1997) Embryonic patterning: to BMP or not to BMP, that is the question. Cell. 89, 171-174.
15. Graff,J.M., Thies,R.S., Song,J.J., Celeste,A.J. and Melton,D.A. (1994) Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo. Cell, 79, 169-179.
16. Harlow,E. and Lane,D. (1988) Antibodies: a Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
17. Heldin,C., Miyazono,K. and ten Dijke,P. (1997) TGF-β signaling from cell membrane to nucleus through SMAD proteins. Nature, 390, 465-471.
18. Hemmati-Brivanlou,A. and Melton,D.A. (1992) A truncated activin receptor inhibits mesoderm induction and formation of axial structures in Xenopus embryos. Nature, 359, 609-614.
19. Hogan,B.L.M. (1996) Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev., 10, 1580-1594.
20. Hogan,B.L.M., Blessing,M., Winnier,G.E., Suzuki,N. and Jones,C.M. (1994) Growth factors in development: the role of TGF-β related polypeptide signaling molecules in embryogenesis. Development, 53-60.
21. Jean,F., Boudreault,A., Basak,A., Seidah,N.G. and Lazure,C. (1995) Fluorescent peptidyl substrate as an aid in studying the substrate specificity of human prohormone conveiiase PC1 and human furin and designing a potent irreversible inhibitor. J. Biol. Chem., 270, 19225-19231.
22. Jean,F., Stella,K., Thomas,L., Liu,G., Xiang,Y., Reason,A.J. and Thomas,G. (1998) α1-Antitrypsin Portland, a bioengineered serpin highly selective fo furin: Application as an antipathogenic agent. Proc. Natl Acad. Sci. USA, 95, 7293-7298.
23. Joseph,E.M. and Melton,D.A. (1997) Xnr4: a Xenopus nodal-related gene expressed in the Spemann Organizer. Dev. Biol., 184, 367-372.
24. Jones,E.A. and Woodland,H.R. (1987) The development of animal cap cells in Xenopus: A measure of the start of animal cap competence to form mesoderm. Development, 101, 557-563.
25. Jones,C.M., Kuehn,M.R., Hogan,B.L.M., Smith,J.C. and Wright,C.V.E. (1995) Nodal-related signals induce axial mesoderm and dorsalize mesoderm during gastrulation. Development, 121, 3651-3662.
26. Jones,C.M., Armes,N. and Smith,J.C. (1996) Signalling by TGF-β family members: short-range effects of Xnr-2 and BMP-4 contrast with the long-range effects of activin. Curr. Biol., 6, 1468-1475.
27. Kengaku,M. and Okamoto,H. (1995) bFGF as a possible morphogen for the anterioposterior axis of the central nervous system. Development, 121, 3121-3130.
28. Kessler,D.S. and Melton,D.A. (1995) Induction of dorsal mesoderm by soluble, mature Vglprotein. Development, 121, 2155-2164.
29. Kintner,C. and Brockes,J.P. (1984) Monoclonal antibodies identify blastemal cells derived from dedifferentiating muscle in newt limb regeneration. Nature, 308, 67-69.
30. Knight,C.G. (1995) Active-site titration of peptidases. Methods Enzymol., 248, 85-101.
31. Korner,J., Chun,J., O'Bryan,L. and Axel,R. (1991) Prohormone processing in Xenopus oocytes: characterization of cleavage signals and cleavage enzymes. Proc. Natl Acad. Sci. USA, 88, 11393-11397.
32. Krieg,P.A. and Melton,D.A. (1984) Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res., 12, 7057-7070.
33. Massagué,J., Hata,A. and Liu,F. (1997) TGFβ signaling through the Smad pathway. Trends Cell Biol., 7, 187-192.
34. Mbikay,M. et al. (1997) Impaired fertility in mice deficient for the testicular germ-cell protease PC4. Proc. Natl Acad. Sci. USA, 94, 6842-6846.
35. Molloy,S.S., Bresnahan,P.A., Leppla,S.H., Klimpel,K.R. and Thomas,G. (1992) Human furin is a calcium-dependent serine endoproteuse that recognizes the sequence Arg-X-X-Arg and efficiently cleaves anthrax toxin protective antigen. J. Biol. Chem., 267, 16396-16402.
36. Molloy,S.S., Thomas,L., VanSlyke,J.K., Stenberg,P.E. and Thomas,G. (1994) Intracellular trafficking and activation of the furin proprotein convertase: localization to the TGN and recycling from the cell surface. EMBO J., 13, 18-33.
37. Moon,R.T. and Christian,J.L. (1989) Microinjection and expression of synthetic mRNAs in Xenopus embryos. Technique, 1, 76-89.
38. Nakayama,K. (1997) Furin: a mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins. Biochem. J., 327, 625-635.
39. Nakayama,K., Kim,W.S., Torii,S., Hosaka,M., Nakagawa,T., Ikemisu,J., Baba,T. and Murakami,K. (1992) Identification of the fourth member of the mammalian endoprotease family homologous to the yeast kex2 protease: its testis specific expression. J. Biol. Chem., 267, 5897-5900.
40. Nakayama,T., Synder,M.A., Grewal,S.S., Tsuneizumi,K., Tabata,T. and Christian,J.L. (1998) Xenopus Smad8 acts downstream of BMP-4 to modulate its activity during vertebrate embryonic patterning. Development, 125, 857-867.
41. Nieuwkoop,P.D. and Faber,J. (1967) Normal table of Xenopus laevis. North Holland Publishing Co., Amsterdam.
42. Seidah,N.G. and Chrétien,M. (1997) Eukaryotic protein processing: endoproteolysis of precursor proteins. Curr. Opin. Biotechnol., 8, 602-607.
43. Smith,W.C., McKendry,R., Ribisi,S.,Jr. and Harland,R.M. (1995) A nodal-related gene defines a physical and functional domain within the Spemann Organizer. Cell, 82, 37-46.
44. Steiner,D.F., Smeekens,S.R. Ohagi,S. and Chan,S.J. (1992) The new enzymology of precursor processing endoproteases. J. Biol. Chem., 267, 23435-23438.
45. Thacker,C., Peters,K., Srayko,M. and Rose,A.M. (1995) The bli-4 locus of Caenorhabditis elegans encodes structurally distinct kex2/subtilisinlike endoproteases essential for early development and adult morphology. Genes Dev., 9, 956-971.
46. Turner,D.L. and Weintraub,H. (1994) Expression of achaete-Schue homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev., 8, 1434-1447.
47. Vize,P.D. and Thomsen,G.H. (1994) Vg1 and regional specification in vertebrates: a new role for an old molecule. Trends Genet., 10, 371-376.
48. Wilson,P.A. and Hemmuti-Brivanlou,A. (1997) Vertebrate neural induction: inducers, inhibitors, and a new synthesis. Neuron, 18, 699-710.
49. Wright,C.V., Morita,E.A., Wilkin,D.J. and DeRobertis,E.M. (1990) The Xenopus XlHbox6 homeoprotein, a marker of posterior neural inducer, is expressed in proliferating neurons. Development, 109, 225-234.
50. Wu,J.Y., Wen,L., Zhang,W. and Rao,Y. (1996) The secreted product of Xenopus gene lunatic Fringe, a vertebrate signaling molecule. Science, 273, 355-358.
51. Zheng,M., Streck,R.D., Scott,R.E.M., Seidah,N.G. and Pintar,J.E. (1994) The developmental expression in rat of proteases furin, PC1, PC2 and carboxypeptidase E: Implications for early maturation of proteolytic processing capacity. J. Neurosci., 14, 4656-4673.
52. Zheng,M., Seidah,N.G. and Pintar,J.E. (1997) The developmental expression in the rat CNSand peripheral tissues of proteases PC5 and PACE-4 mRNAs: comparison with other proprotein processing enzymes. Dev. Biol., 181, 268-283.