Home LiteratureArticle Details
PMID: 9363949 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Cleavage of Chordin by Xolloid metalloprotease suggests a role for proteolytic processing in the regulation of Spemann organizer activity.

Cell ·Vol. 91 ·No. 3 ·1997-10-31 ·Pages 407-16

Piccolo S, Agius E, Lu B, Goodman S, Dale L, De Robertis EM

Abstract

The Xolloid secreted metalloprotease, a tolloid-related protein, was found to cleave Chordin and Chordin/BMP-4 complexes at two specific sites in biochemical experiments Xolloid mRNA blocks secondary axes caused by chordin, but not by noggin, follistatin, or dominant-negative BMP receptor, mRNA injection. Xolloid-treated Chordin protein was unable to antagonize BMP activity. Furthermore, Xolloid digestion released biologically active BMPs from Chordin/BMP inactive complexes. Injection of dominant-negative Xolloid mRNA indicated that the in vivo function of Xolloid is to limit the extent of Spemann's organizer field. We propose that Xolloid regulates organizer function by a novel proteolytic mechanism involving a double inhibition pathway required to pattern the dorsoventral axis: [formula in text].

MeSH Terms
Amino Acid Sequence Animals Bone Morphogenetic Protein 4 Bone Morphogenetic Protein 7 Bone Morphogenetic Proteins/metabolism Ectoderm Glycoproteins/metabolism Intercellular Signaling Peptides and Proteins Mesoderm Metalloendopeptidases/metabolism Molecular Sequence Data RNA, Messenger Substrate Specificity Transforming Growth Factor beta Xenopus Proteins
Chemicals
Bone Morphogenetic Protein 4 Bone Morphogenetic Protein 7 Bone Morphogenetic Proteins Glycoproteins Intercellular Signaling Peptides and Proteins RNA, Messenger Transforming Growth Factor beta Xenopus Proteins bmp4 protein, Xenopus bmp7.1 protein, Xenopus chordin Metalloendopeptidases TLL2 protein, Xenopus
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Piccolo S
Howard Hughes Medical Institute, Department of Biological Chemistry, University of California, Los Angeles 90095-1662, USA.
Agius E
Lu B
Goodman S
Dale L
De Robertis E M
References (45)
45 references, click to expand
  1. Decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo.
    Cell. 1992 Oct 30;71(3):451-61 PMID: 1423606
  2. Bone morphogenetic protein 4: a ventralizing factor in early Xenopus development.
    Development. 1992 Jun;115(2):573-85 PMID: 1425340
  3. DVR-4 (bone morphogenetic protein-4) as a posterior-ventralizing factor in Xenopus mesoderm induction.
    Development. 1992 Jun;115(2):639-47 PMID: 1425343
  4. Genes for bone morphogenetic proteins are differentially transcribed in early amphibian embryos.
    Biochem Biophys Res Commun. 1992 Aug 14;186(3):1487-95 PMID: 1510675
  5. Localized enhancement and repression of the activity of the TGF-beta family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo.
    Development. 1992 Mar;114(3):583-97 PMID: 1618130
  6. In situ hybridization: an improved whole-mount method for Xenopus embryos.
    Methods Cell Biol. 1991;36:685-95 PMID: 1811161
  7. The Drosophila dorsal-ventral patterning gene tolloid is related to human bone morphogenetic protein 1.
    Cell. 1991 Nov 1;67(3):469-81 PMID: 1840509
  8. Mutations affecting the pattern of the larval cuticle inDrosophila melanogaster : II. Zygotic loci on the third chromosome.
    Wilehm Roux Arch Dev Biol. 1984 Sep;193(5):283-295 PMID: 28305338
  9. short gastrulation, a mutation causing delays in stage-specific cell shape changes during gastrulation in Drosophila melanogaster.
    Dev Biol. 1988 Oct;129(2):417-27 PMID: 3138149
  10. Novel regulators of bone formation: molecular clones and activities.
    Science. 1988 Dec 16;242(4885):1528-34 PMID: 3201241
  11. Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo.
    Cell. 1994 Oct 7;79(1):169-79 PMID: 7522972
  12. Ventral mesodermal patterning in Xenopus embryos: expression patterns and activities of BMP-2 and BMP-4.
    Dev Genet. 1995;17(1):78-89 PMID: 7554498
  13. Mutational analysis of the Drosophila tolloid gene, a human BMP-1 homolog.
    Development. 1994 Apr;120(4):861-70 PMID: 7600963
  14. A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin.
    Nature. 1995 Jul 20;376(6537):249-53 PMID: 7617035
  15. Induction of epidermis and inhibition of neural fate by Bmp-4.
    Nature. 1995 Jul 27;376(6538):331-3 PMID: 7630398
  16. Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus.
    Nature. 1995 Jul 27;376(6538):333-6 PMID: 7630399
  17. The metzincins--topological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a superfamily of zinc-peptidases.
    Protein Sci. 1995 May;4(5):823-40 PMID: 7663339
  18. Efficient expression of a heterodimer of bone morphogenetic protein subunits using a baculovirus expression system.
    Biochem Biophys Res Commun. 1995 Apr 26;209(3):859-66 PMID: 7733977
  19. Xenopus chordin and Drosophila short gastrulation genes encode homologous proteins functioning in dorsal-ventral axis formation.
    Cell. 1995 Jan 13;80(1):19-20 PMID: 7813014
  20. A truncated bone morphogenetic protein receptor affects dorsal-ventral patterning in the early Xenopus embryo.
    Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10255-9 PMID: 7937936
  21. On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo.
    EMBO J. 1994 Nov 1;13(21):5015-25 PMID: 7957067
  22. Two domains of the tolloid protein contribute to its unusual genetic interaction with decapentaplegic.
    Dev Biol. 1994 Mar;162(1):209-20 PMID: 8125188
  23. Cloning and expression of cDNA encoding Xenopus laevis bone morphogenetic protein-1 during early embryonic development.
    Gene. 1993 Dec 8;134(2):257-61 PMID: 8262384
  24. An activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo.
    Development. 1993 Feb;117(2):807-22 PMID: 8330541
  25. Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo.
    Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2905-9 PMID: 8464906
  26. Bone morphogenetic protein-1: the type I procollagen C-proteinase.
    Science. 1996 Jan 19;271(5247):360-2 PMID: 8553073
  27. A common plan for dorsoventral patterning in Bilateria.
    Nature. 1996 Mar 7;380(6569):37-40 PMID: 8598900
  28. Characterization of a novel gene product (mammalian tolloid-like) with high sequence similarity to mammalian tolloid/bone morphogenetic protein-1.
    Genomics. 1996 Jun 1;34(2):157-65 PMID: 8661043
  29. Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4.
    Cell. 1996 Aug 23;86(4):589-98 PMID: 8752213
  30. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4.
    Cell. 1996 Aug 23;86(4):599-606 PMID: 8752214
  31. The Xenopus dorsalizing factor noggin ventralizes Drosophila embryos by preventing DPP from activating its receptor.
    Cell. 1996 Aug 23;86(4):607-17 PMID: 8752215
  32. Genetic analysis of dorsoventral pattern formation in the zebrafish: requirement of a BMP-like ventralizing activity and its dorsal repressor.
    Genes Dev. 1996 Oct 1;10(19):2452-61 PMID: 8843197
  33. The Drosophila short gastrulation gene prevents Dpp from autoactivating and suppressing neurogenesis in the neuroectoderm.
    Genes Dev. 1996 Nov 15;10(22):2922-34 PMID: 8918893
  34. Failure of ventral body wall closure in mouse embryos lacking a procollagen C-proteinase encoded by Bmp1, a mammalian gene related to Drosophila tolloid.
    Development. 1996 Nov;122(11):3587-95 PMID: 8951074
  35. dino and mercedes, two genes regulating dorsal development in the zebrafish embryo.
    Development. 1996 Dec;123:95-102 PMID: 9007232
  36. Vertebrate embryonic cells will become nerve cells unless told otherwise.
    Cell. 1997 Jan 10;88(1):13-7 PMID: 9019398
  37. XBMP-1B (Xtld), a Xenopus homolog of dorso-ventral polarity gene in Drosophila, modifies tissue phenotypes of ventral explants.
    Dev Growth Differ. 1997 Feb;39(1):43-51 PMID: 9079034
  38. Embryonic patterning: to BMP or not to BMP, that is the question.
    Cell. 1997 Apr 18;89(2):171-4 PMID: 9108472
  39. Structurally related receptors and antagonists compete for secreted Wnt ligands.
    Cell. 1997 Mar 21;88(6):725-8 PMID: 9118212
  40. Mesoderm induction by BMP-4 and -7 heterodimers.
    Biochem Biophys Res Commun. 1997 Mar 6;232(1):153-6 PMID: 9125121
  41. The dorsalizing and neural inducing gene follistatin is an antagonist of BMP-4.
    Mech Dev. 1997 Apr;63(1):39-50 PMID: 9178255
  42. Bmp-4 acts as a morphogen in dorsoventral mesoderm patterning in Xenopus.
    Development. 1997 Jun;124(12):2325-34 PMID: 9199359
  43. The zebrafish organizer requires chordino.
    Nature. 1997 Jun 26;387(6636):862-3 PMID: 9202118
  44. Production of a DPP activity gradient in the early Drosophila embryo through the opposing actions of the SOG and TLD proteins.
    Cell. 1997 Oct 31;91(3):417-26 PMID: 9363950
  45. BMP1-related metalloproteinases promote the development of ventral mesoderm in early Xenopus embryos.
    Dev Biol. 1998 Mar 15;195(2):144-57 PMID: 9520331
Article Info
Journal
Cell
Abbr.
Cell
ISSN
0092-8674
DOI
10.1016/s0092-8674(00)80424-9
Published
1997-10-31
Pages
407-16
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC3070600
Subset
IM
Grants
NICHD NIH HHS · R37 HD021502 · United States
NICHD NIH HHS · R37 HD021502-13 · United States
NICHD NIH HHS · R37 HD21502-11 · United States
External Links
PubMed source DOI: 10.1016/s0092-8674(00)80424-9 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2