Advertisement
JOURNAL ARTICLES
Failure of ventral body wall closure in mouse embryos lacking a procollagen C-proteinase encoded by Bmp1, a mammalian gene related to Drosophila tolloid
N. Suzuki, P.A. Labosky, Y. Furuta, L. Hargett, R. Dunn, A.B. Fogo, K. Takahara, D.M. Peters, D.S. Greenspan, B.L. Hogan
Development 1996 122: 3587-3595;

Summary

The mouse bone morphogenetic protein1 (Bmp1) gene encodes a secreted astacin metalloprotease that cleaves the COOH-propeptide of procollagen I, II and III. BMP-1 is also related to the product of the Drosophila patterning gene, tolloid (tld), which enhances the activity of the TGFbeta-related growth factor Decapentaplegic and promotes development of the dorsalmost amnioserosa. We have disrupted the mouse Bmp1 gene by deleting DNA sequences encoding the active site of the astacin-like protease domain common to all splice variants. Homozygous mutant embryos appear to have a normal skeleton, apart from reduced ossification of certain skull bones. However, they have a persistent herniation of the gut in the umbilical region and do not survive beyond birth. Analysis of the amnion of homozygous mutant embryos reveals the absence of the fold that normally tightly encloses the physiological hernia of the gut. At the electron microscopic level, the extracellular matrix of the amnion contains collagen fibrils with an abnormal morphology, consistent with the incorporation of partially processed procollagen molecules. Metabolical labelling and immunofluorescence studies also reveal abnormal processing and deposition of procollagen by homozygous mutant fibroblasts in culture.

Reference

    1. Arora K.,
    2. Nusslein-Volhard C.
    (1992) Altered mitotic domains reveal fate map changes in Drosophila embryos mutant for zygotic dorsoventral patterning genes. Development 114, 1003–1024
    OpenUrlAbstract
    1. Bernstein E. F.,
    2. Chen Y. Q.,
    3. Kopp J. B.,
    4. Fisher L. W.,
    5. Brown D.,
    6. Lakkakorpi J.,
    7. Robey F. A.,
    8. Uitto J.
    (1996) Chronic sun-exposure alters the collagen of the superficial dermis: evaluation by Northern analysis, immunohistochemical staining and confocal scanning laser microscopy. J. Am. Acad. Dermatol 34, 209–218
    OpenUrlCrossRefPubMedWeb of Science
    1. Bode W.,
    2. Gomis-Ruth F. X.,
    3. Huber R.,
    4. Zwilling R.,
    5. Stocker W.
    (1992) Structure of astacin and implications for activation of astacins and zinc-ligation of collagenases. Nature 358, 164–167
    OpenUrlCrossRefPubMed
    1. Childs S. R.,
    2. O'Connor M. B.
    (1994) Two domains of the tolloid protein contribute to its unusual genetic interaction with decapentaplegic. Dev. Biol 162, 209–220
    OpenUrlCrossRefPubMedWeb of Science
    1. Dumermuth E.,
    2. Sterchi E. E.,
    3. Jiang W.,
    4. Wolz R. L.,
    5. Bond J. S.,
    6. Flannery A. V.,
    7. Beynon R. J.
    (1991) The Astacin family of metalloendopeptidases. J. Biol. Chem 266, 21381–21385
    OpenUrlAbstract/FREE Full Text
    1. Dzamba B. J.,
    2. Wu H.,
    3. Jaenisch R.,
    4. Peters D. M.
    (1993) Fibronectin binding site in type I collagen in fibroblast culture. Biochem. J 245, 677–682
    OpenUrl
    1. Ferguson E. L.,
    2. Anderson K. V.
    (1992) Localized enhancement and repression of the activity of the TGFfamily member, decapentaplegic, is necessary for dorsal-ventral pettern formation in the Drosophila embryo. Development 114, 583–597
    OpenUrlAbstract
    1. Finelli A. L.,
    2. Bossie C. A.,
    3. Xie T.,
    4. Padgett R. W.
    (1994) Mutational analysis of the Drosophila tolloid gene, a human BMP-1 homolog. Development 120, 861–870
    OpenUrlAbstract
    1. Finelli A. L.,
    2. Xie T.,
    3. Bossie C. A.,
    4. Blackman R. K.,
    5. Padgett R. W.
    (1995) The tolkin gene is a tolloid/BMP-1 homolog that is essential for Drosophila development. Genetics 141, 271–281
    OpenUrlAbstract/FREE Full Text
    1. Francois V.,
    2. Bier E.
    (1995) Xenopus chordin and Drosophila short gastrulation genes encode homologous proteins functioning in dorsal-ventral axis formation. Cell 80, 19–20
    OpenUrlCrossRefPubMedWeb of Science
    1. Fukagawa M.,
    2. Suzuki N.,
    3. Hogan B. L. M.,
    4. Jones C. M.
    (1994) Embryonic expression of mouse bone morphogenetic protein-1 (BMP-1) which is related to the Drosophila dorsoventral gene tolloid and encodes a putative astacin metalloendopeptidase. Dev. Biol 163, 175–183
    OpenUrlCrossRefPubMedWeb of Science
    1. Hogan B. L. M.
    (1996) Bone morphogenetic proteins: multifunctional regulators of embryonic development. Genes Dev 10, 1580–1594
    OpenUrlFREE Full Text
    1. Holley S. A.,
    2. Jackson P. D.,
    3. Sasai Y.,
    4. Lu B.,
    5. De Robertis E. M.,
    6. Hoffmann F. M.,
    7. Ferguson E. L.
    (1995) A conserved system for dorsal-ventral patterning in insects and vertebrate involving sog and chordin. Nature 376, 249–253
    OpenUrlCrossRefPubMedWeb of Science
    1. Hwang S.-P. L.,
    2. Partin J. S.,
    3. Lennarz W. J.
    (1994) Characterization of a homolog of human bone morphogenetic protein 1 in the embryo of the sea urchin, Strongylocentrotus purpuratus. Development 120, 559–568
    OpenUrlAbstract
    1. Karlsson O.,
    2. Thor S.,
    3. Norberg T.,
    4. Ohlsson H.,
    5. Edlund T.
    (1990) Insulin gene enhancer binding protein Isl-1 is a member of a novel class of proteins containing both a homeo-and a Cys-His domain. Nature 344, 879–882
    OpenUrlCrossRefPubMedWeb of Science
    1. Kessler E.,
    2. Takahara K.,
    3. Biniaminov L.,
    4. Brusel M.,
    5. Greenspan D. S.
    (1996) Bone morphogenetic protein-1: The Type 1 procollagen C-proteinase. Science 271, 360–362
    OpenUrlAbstract
    1. Lee S.-T.,
    2. Kessler E.,
    3. Greenspan D. S.
    (1990) Analysis of site-directed mutations in human pro-2(I) collagen which block cleavage by the C-proteinase. J. Biol. Chem 265, 21992–21996
    OpenUrlAbstract/FREE Full Text
    1. Li S.-W.,
    2. Sieron A. L.,
    3. Fertala A.,
    4. Hojima Y.,
    5. Arnold W. V.,
    6. Prockop D. J.
    (1996) The C-proteinase that processes procollagens to fibrillar collagens is identical to the protein previously identified as bone morphogenetic protein-1. Proc. Natl. Acad. Sci. USA 93, 5127–5130
    OpenUrlAbstract/FREE Full Text
    1. Maeno M.,
    2. Xue Y.,
    3. Wood T. I.,
    4. Ong R. C.,
    5. Kung H.
    (1993) Cloning and expression of CDNA encoding Xenopus laevis bone morphogenetic protein-1 during early embryonic development. Gene 134, 257–261
    OpenUrlCrossRefPubMedWeb of Science
    1. Nguyen T.,
    2. Jamal J.,
    3. Shimell M. J.,
    4. Arora K.,
    5. O'Connor M.
    (1994) Characterization of tolloid-related-1: a BMP-1-like product that is required during larval and pupal stages of Drosophila development. Dev. Biol 166, 569–586
    OpenUrlCrossRefPubMedWeb of Science
    1. Panchenko M. V.,
    2. Stetler-Stevenson W. G.,
    3. Trubetskoy O. V.,
    4. Gacheru S. N.,
    5. Kagen H. M.
    (1996) Metalloproteinase activity secreted by fibrogenic cells in the processing of prolysyl oxidase: potential role of procollagen C-proteinase. J. Biol. Chem 271, 7113–7119
    OpenUrlAbstract/FREE Full Text
    1. Reynolds S. D.,
    2. Angerer L. M.,
    3. Palis J.,
    4. Nasir A.,
    5. Angerer R. C.
    (1992) Early mRNAs, spatially restricted along the animal-vegetal axis of sea urchin embryos, including one encoding a protein related to tolloid and BMP-1. Development 114, 769–786
    OpenUrlAbstract
    1. Rudniki M. A.,
    2. Braun T.,
    3. Hinuma S.,
    4. Jaenisch R.
    (1992) Inactivation of MyoD in mice leads tpo up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71, 383–390
    OpenUrlCrossRefPubMedWeb of Science
    1. Salinas C. F.,
    2. Bartoshesky L.,
    3. Otherson H. B.,
    4. Leape L.,
    5. Feingold M.,
    6. Jorgenson R. J.
    (1979) Familial occurrence of gastroschisis. Am. J. Dis. Child 133, 514–517
    OpenUrlCrossRefPubMed
    1. Sasaki H.,
    2. Hogan B. L. M.
    (1994) HNF-3as a regulator of floorplate development. Cell 76, 103–115
    OpenUrlCrossRefPubMedWeb of Science
    1. Shimell M. J.,
    2. Ferguson E. L.,
    3. Childs S. R.,
    4. O'Connor M. B.
    (1991) The Drosophila dorsal-ventral patterning gene tolloid is related to human bone morphogenetic protein 1. Cell 67, 469–481
    OpenUrlCrossRefPubMedWeb of Science
    1. Takahara K.,
    2. Lyons G. E.,
    3. Greenspan D. S.
    (1994) Bone morphogenetic protein-1 and a mammalian tolloid homologue (mTld) are encoded by alternatively spliced transcripts which are differentially expressed in some tissues. J. Biol. Chem 269, 32572–32578
    OpenUrlAbstract/FREE Full Text
    1. Takahara K.,
    2. Lee S.,
    3. Wood S.,
    4. Greenspan D. S.
    (1995) Structural organisization and genetic localization of the human bone morphogenetic protein 1/mammalian tolloid gene. Genomics 29, 9–15
    OpenUrlCrossRefPubMedWeb of Science
    1. Takahara K.,
    2. Brevard R.,
    3. Hoffman G. G.,
    4. Suzuki N.,
    5. Greenspan D. S.
    (1996) Characterization of a novel gene product (mammalian tolloid-like) with high sequence similarity to mammalian tolloid/bone morphogenetic protein-1. Genomics 34, 157–165
    OpenUrlCrossRefPubMedWeb of Science
    1. Thor S.,
    2. Ericson J.,
    3. Brannestrom T.,
    4. Edlund T.
    (1991) The homeodomain LIM Protein Isl-1 is expressed in subsets of neurons and endocrine cells in the adult rat. Neuron 7, 881–889
    OpenUrlCrossRefPubMedWeb of Science
    1. Winnier G.,
    2. Blessing M.,
    3. Labosky P. A.,
    4. Hogan B. L. M.
    (1995) Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes and Development 9, 2105–2116
    OpenUrlAbstract/FREE Full Text
    1. Wozney J. M.,
    2. Rosen V.,
    3. Celeste A. J.,
    4. Mitsock L. M.,
    5. Whitters M. J.,
    6. Kris R. W.,
    7. Hewick R. M.,
    8. Wang E. A.
    (1988) Novel regulators of bone formation: molecular clones and activities. Science 242, 1528–1534
    OpenUrlAbstract/FREE Full Text
    1. Yan L.,
    2. Pollock G. H.,
    3. Nagase H.,
    4. Sarras J. M. P.
    (1995). A 25.7103 Mr hydra metalloproteinase (HMP1), a member of the astacin family, localizes to the extracellular matrix of Hydra vulgaris in a head-specific manner and has a developmental function. Development 121, 1591–1602
    OpenUrlAbstract
Back to top

 Download PDF

Email
JOURNAL ARTICLES
Failure of ventral body wall closure in mouse embryos lacking a procollagen C-proteinase encoded by Bmp1, a mammalian gene related to Drosophila tolloid
N. Suzuki, P.A. Labosky, Y. Furuta, L. Hargett, R. Dunn, A.B. Fogo, K. Takahara, D.M. Peters, D.S. Greenspan, B.L. Hogan
Development 1996 122: 3587-3595;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Alerts

Article navigation

Other journals from The Company of Biologists

Advertisement

The people behind the papers – George Britton and Aryeh Warmflash

George and Aryeh

First author George Britton and his supervisor Aryeh Warmflash discuss their new Development paper in which they apply advanced in vitro culturing techniques to investigate embryonic ectoderm patterning.

Travelling Fellowship – New imaging approach unveils a bigger picture

Highlights from Travelling Fellowship trips

Find out how Pamela Imperadore’s Travelling Fellowship grant from The Company of Biologists took her to Germany, where she used new imaging techniques to investigate the cellular machinery underlying octopus arm regeneration. Don’t miss the next application deadline for 2020 travel, coming up on 29 November. Where will your research take you?

Protein function can be controlled by light using optogenetic techniques. In their new Primer, Stefano De Renzis and his colleagues in Heidelberg provide an overview of the most commonly used optogenetic tools and their application in developmental biology.

preLights – Self-organised symmetry breaking in zebrafish reveals feedback from morphogenesis to pattern formation

Sundar Naganathan

preLighter Sundar Naganathan explains his selected preprint by Vikas Trivedi, Benjamin Steventon and their co-workers on pescoids, a new in vitro model system to study early zebrafish embryogenesis.

Spotlight – Can laboratory model systems instruct human limb regeneration?

An extract from a schematic demonstrating the possible pipeline for how discovery in lab model systems can influence applications for regenerative therapies.

One of the most challenging objectives of tissue regeneration research is regrowth of a lost or amputated limb. Here, Ben Cox, Maximina Yun and Kenneth Poss outline the research avenues yet to be explored to move closer to this capstone achievement.

Articles of interest in our sister journals

Tox4 modulates cell fate reprogramming

Lotte Vanheer, Juan Song, Natalie De Geest, Adrian Janiszewski, Irene Talon, Caterina Provenzano, Taeho Oh, Joel Chappell, Vincent Pasque
Journal of Cell Science

Drosophila melanogaster: a simple system for understanding complexity

Stephanie E. Mohr, Norbert Perrimon
Disease Models & Mechanisms