» Articles » PMID: 29974861

Apical and Basal Matrix Remodeling Control Epithelial Morphogenesis

Overview
Journal Dev Cell
Publisher Cell Press
Date 2018 Jul 6
PMID 29974861
Citations 41
Authors
Affiliations
Soon will be listed here.
Abstract

Epithelial tissues can elongate in two dimensions by polarized cell intercalation, oriented cell division, or cell shape change, owing to local or global actomyosin contractile forces acting in the plane of the tissue. In addition, epithelia can undergo morphogenetic change in three dimensions. We show that elongation of the wings and legs of Drosophila involves a columnar-to-cuboidal cell shape change that reduces cell height and expands cell width. Remodeling of the apical extracellular matrix by the Stubble protease and basal matrix by MMP1/2 proteases induces wing and leg elongation. Matrix remodeling does not occur in the haltere, a limb that fails to elongate. Limb elongation is made anisotropic by planar polarized Myosin-II, which drives convergent extension along the proximal-distal axis. Subsequently, Myosin-II relocalizes to lateral membranes to accelerate columnar-to-cuboidal transition and isotropic tissue expansion. Thus, matrix remodeling induces dynamic changes in actomyosin contractility to drive epithelial morphogenesis in three dimensions.

Citing Articles

3D Micropatterned Traction Force Microscopy: A Technique to Control 3D Cell Shape While Measuring Cell-Substrate Force Transmission.

Faure L, Gomez-Gonzalez M, Baguer O, Comelles J, Martinez E, Arroyo M Adv Sci (Weinh). 2024; 11(46):e2406932.

PMID: 39443837 PMC: 11633470. DOI: 10.1002/advs.202406932.


Active shape programming drives wing disc eversion.

Fuhrmann J, Krishna A, Paijmans J, Duclut C, Cwikla G, Eaton S Sci Adv. 2024; 10(32):eadp0860.

PMID: 39121221 PMC: 11637009. DOI: 10.1126/sciadv.adp0860.


Unveiling the cell dynamics during the final shape formation of the tarsus in Drosophila adult leg by live imaging.

Hiraiwa S, Takeshita S, Terano T, Hayashi R, Suzuki K, Tajiri R Dev Genes Evol. 2024; 234(2):117-133.

PMID: 38977431 PMC: 11611951. DOI: 10.1007/s00427-024-00719-z.


Lens placode modulates extracellular matrix formation during early eye development.

De Magalhaes C, Cvekl A, Jaeger R, Yan C Differentiation. 2024; 138:100792.

PMID: 38935992 PMC: 11247415. DOI: 10.1016/j.diff.2024.100792.


Dynamic interplay of microtubule and actomyosin forces drive tissue extension.

Singh A, Thale S, Leibner T, Lamparter L, Ricker A, Nusse H Nat Commun. 2024; 15(1):3198.

PMID: 38609383 PMC: 11014958. DOI: 10.1038/s41467-024-47596-8.


References
1.
LEWIS E . A gene complex controlling segmentation in Drosophila. Nature. 1978; 276(5688):565-70. DOI: 10.1038/276565a0. View

2.
Roy S, Ernst J, Kharchenko P, Kheradpour P, Negre N, Eaton M . Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science. 2010; 330(6012):1787-97. PMC: 3192495. DOI: 10.1126/science.1198374. View

3.
Butler L, Blanchard G, Kabla A, Lawrence N, Welchman D, Mahadevan L . Cell shape changes indicate a role for extrinsic tensile forces in Drosophila germ-band extension. Nat Cell Biol. 2009; 11(7):859-64. DOI: 10.1038/ncb1894. View

4.
Ward R, Evans J, Thummel C . Genetic modifier screens in Drosophila demonstrate a role for Rho1 signaling in ecdysone-triggered imaginal disc morphogenesis. Genetics. 2003; 165(3):1397-415. PMC: 1462826. DOI: 10.1093/genetics/165.3.1397. View

5.
Fristom D, Fristom J . The mechanism of evagination of imaginal discs of Drosophila melanogaster. 1. General considerations. Dev Biol. 1975; 43(1):1-23. DOI: 10.1016/0012-1606(75)90127-x. View