A luminal glycoprotein drives dose-dependent diameter expansion of the Drosophila melanogaster hindgut tube

Autor: Tina M. Chavoshi, Anne Uv, Erika Tång, Anne-Laure Bougé, Zulfeqhar A. Syed, Iris F. van Dijk-Härd, Sunitha Byri, Hervé Bouhin
Přispěvatelé: Centre des Sciences du Goût et de l'Alimentation [Dijon] ( CSGA ), Institut National de la Recherche Agronomique ( INRA ) -Université de Bourgogne ( UB ) -AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Centre National de la Recherche Scientifique ( CNRS ), Centre des Sciences du Goût et de l'Alimentation [Dijon] (CSGA), Institut National de la Recherche Agronomique (INRA)-Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Centre National de la Recherche Scientifique (CNRS)
Jazyk: angličtina
Rok vydání: 2012
Předmět:
glycoprotein
Cancer Research
hindgut
Organogenesis
[ SDV.AEN ] Life Sciences [q-bio]/Food and Nutrition
tenectin
Hydrostatic pressure
Extracellular matrix
lumen
Molecular Cell Biology
Morphogenesis
Drosophila Proteins
epithelial tube
Genetics (clinical)
Animal biology
Extracellular Matrix Proteins
Drosophila Melanogaster
Gene Expression Regulation
Developmental
Hindgut
Animal Models
Anatomy
musculoskeletal system
Extracellular Matrix
Cell biology
medicine.anatomical_structure
Alimentation et Nutrition
Research Article
lcsh:QH426-470
Lumen (anatomy)
Biology
Model Organisms
Genetic Mutation
Biologie animale
Genetics
medicine
Animals
Food and Nutrition
Molecular Biology
Ecology
Evolution
Behavior and Systematics
Glycoproteins
Embryonic stem cell
Extracellular Matrix Composition
Epithelium
Gastrointestinal Tract
lcsh:Genetics
Mutagenesis
Ectopic expression
Gene Function
[SDV.AEN]Life Sciences [q-bio]/Food and Nutrition
Organism Development
Developmental Biology
Zdroj: Plos Genetics 8 (8), 1-14. (2012)
PLoS Genetics
PLoS Genetics, Public Library of Science, 2012, 8 (8), pp.e1002850. 〈10.1371/journal.pgen.1002850〉
PLoS Genetics, Vol 8, Iss 8, p e1002850 (2012)
PLoS Genetics, Public Library of Science, 2012, 8 (8), pp.e1002850. ⟨10.1371/journal.pgen.1002850⟩
ISSN: 1553-7390
1553-7404
DOI: 10.1371/journal.pgen.1002850〉
Popis: An important step in epithelial organ development is size maturation of the organ lumen to attain correct dimensions. Here we show that the regulated expression of Tenectin (Tnc) is critical to shape the Drosophila melanogaster hindgut tube. Tnc is a secreted protein that fills the embryonic hindgut lumen during tube diameter expansion. Inside the lumen, Tnc contributes to detectable O-Glycans and forms a dense striated matrix. Loss of tnc causes a narrow hindgut tube, while Tnc over-expression drives tube dilation in a dose-dependent manner. Cellular analyses show that luminal accumulation of Tnc causes an increase in inner and outer tube diameter, and cell flattening within the tube wall, similar to the effects of a hydrostatic pressure in other systems. When Tnc expression is induced only in cells at one side of the tube wall, Tnc fills the lumen and equally affects all cells at the lumen perimeter, arguing that Tnc acts non-cell-autonomously. Moreover, when Tnc expression is directed to a segment of a tube, its luminal accumulation is restricted to this segment and affects the surrounding cells to promote a corresponding local diameter expansion. These findings suggest that deposition of Tnc into the lumen might contribute to expansion of the lumen volume, and thereby to stretching of the tube wall. Consistent with such an idea, ectopic expression of Tnc in different developing epithelial tubes is sufficient to cause dilation, while epidermal Tnc expression has no effect on morphology. Together, the results show that epithelial tube diameter can be modelled by regulating the levels and pattern of expression of a single luminal glycoprotein.
Author Summary Epithelial tubes constitute the functional units of vital organs, and they undergo highly regulated changes in size and shape during development to accommodate the three-dimensional configurations optimal for organ physiology. Through studies of Drosophila melanogaster, we show that epithelial tube diameter can be modelled simply by regulating the levels and pattern of expression of a single glycoprotein. The protein is secreted into the tubular lumen, where it forms a dense matrix and acts in a dose-dependent manner to drive diameter growth. We suggest that deposition of the protein into the lumen promotes local expansion of the lumen volume, and thereby stretching of the surrounding tube wall. Such a mechanism could represent a general means to adjust tube diameter during epithelial organ development.
Databáze: OpenAIRE
Externí odkaz: