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Gastrulation in the sea urchin embryo requires the deposition of crosslinked collagen within the extracellular matrix.

Publication ,  Journal Article
Wessel, GM; McClay, DR
Published in: Developmental biology
May 1987

This study demonstrates that a collagenous extracellular matrix (ECM) is necessary for gastrulation in the sea urchin embryo. The approach taken was to disrupt collagen processing with two types of agents (a lathyritic agent, beta-aminopropionitrile (BAPN), and three types of proline analogs: dehydroproline, cis-OH-proline, and azetidine carboxylic acid) and to assess the effect on embryogenesis by morphological, immunological, and biochemical criteria. Embryos chronically exposed to either of the agents following fertilization displayed no detectable developmental abnormalities before the mesenchyme blastula stage. These embryos, however, did not gastrulate nor differentiate any further and remained at the mesenchyme blastula stage for at least 36 hr. Upon removal of the agents, the embryos resumed a normal developmental schedule and formed pluteus larvae that were indistinguishable from control embryos. By immunofluorescence studies with monospecific antibodies to type I and type IV collagens it is seen that the lathyritic agent BAPN reduces the accumulation of collagens within the ECM. This effect is confirmed and quantitated by use of an ELISA and by a biochemical determination of OH-proline. When the agents are removed from the inhibited embryos, collagen deposition returns to normal, coincident with gastrulation. Western-blot analysis, using monospecific antibodies to collagen, demonstrates that the effect of the lathyritic agent is to reduce the stability of the extracellular collagen by inhibiting the intra- and intermolecular crosslinking of collagen molecules. BAPN exhibits a dose-dependent effect on morphogenesis, but has no effect on respiration nor on protein synthesis of the embryos throughout development. Although the lathyritic agent affects collagen deposition, it is shown to not affect the expression of other molecules of the ECM, nor that of several cell surface molecules. However, a cell surface molecule that is expressed specifically in the endoderm, termed Endo 1, is not expressed in the inhibited embryos. Endo 1 is expressed after removal of the lathyritic agent and its appearance is coincident with gastrulation in the recovered embryos. These results suggest that a collagenous ECM is important for gastrulation and subsequent differentiation in the sea urchin, but not for earlier developmental processes. In addition, the dependence of Endo 1 expression on the collagenous ECM raises the possibility that this cell surface molecule is in some way regulated by interactions of the presumptive endodermal cells with the ECM.

Duke Scholars

Published In

Developmental biology

DOI

EISSN

1095-564X

ISSN

0012-1606

Publication Date

May 1987

Volume

121

Issue

1

Start / End Page

149 / 165

Related Subject Headings

  • Protein Biosynthesis
  • Oxygen Consumption
  • Morphogenesis
  • Hydroxyproline
  • Gastrula
  • Fluorescent Antibody Technique
  • Fibronectins
  • Extracellular Matrix
  • Developmental Biology
  • Collagen
 

Citation

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Wessel, G. M., & McClay, D. R. (1987). Gastrulation in the sea urchin embryo requires the deposition of crosslinked collagen within the extracellular matrix. Developmental Biology, 121(1), 149–165. https://doi.org/10.1016/0012-1606(87)90148-5
Wessel, G. M., and D. R. McClay. “Gastrulation in the sea urchin embryo requires the deposition of crosslinked collagen within the extracellular matrix.Developmental Biology 121, no. 1 (May 1987): 149–65. https://doi.org/10.1016/0012-1606(87)90148-5.
Wessel, G. M., and D. R. McClay. “Gastrulation in the sea urchin embryo requires the deposition of crosslinked collagen within the extracellular matrix.Developmental Biology, vol. 121, no. 1, May 1987, pp. 149–65. Epmc, doi:10.1016/0012-1606(87)90148-5.
Journal cover image

Published In

Developmental biology

DOI

EISSN

1095-564X

ISSN

0012-1606

Publication Date

May 1987

Volume

121

Issue

1

Start / End Page

149 / 165

Related Subject Headings

  • Protein Biosynthesis
  • Oxygen Consumption
  • Morphogenesis
  • Hydroxyproline
  • Gastrula
  • Fluorescent Antibody Technique
  • Fibronectins
  • Extracellular Matrix
  • Developmental Biology
  • Collagen