Ribbon modulates apical membrane during tube elongation through Crumbs and Moesin

Bilal E. Kerman, Alan M. Cheshire, Monn Monn Myat, Deborah J Andrew

Research output: Contribution to journalArticle

Abstract

Although the formation and maintenance of epithelial tubes are essential for the viability of multicellular organisms, our understanding of the molecular and cellular events coordinating tubulogenesis is relatively limited. Here, we focus on the activities of Ribbon, a novel BTB-domain containing nuclear protein, in the elongation of two epithelial tubes: the Drosophila salivary gland and trachea. We show that Ribbon interacts with Lola Like, another BTB-domain containing protein required for robust nuclear localization of Ribbon, to upregulate crumbs expression and downregulate Moesin activity. Our ultrastructural analysis of ribbon null salivary glands by TEM reveals a diminished pool of subapical vesicles and an increase in microvillar structure, cellular changes consistent with the known role of Crumbs in apical membrane generation and of Moesin in the cross-linking of the apical membrane to the subapical cytoskeleton. Furthermore, the subapical localization of Rab11, a small GTPase associated with apical membrane delivery and rearrangement, is significantly diminished in ribbon mutant salivary glands and tracheae. These findings suggest that Ribbon and Lola Like function as a novel transcriptional cassette coordinating molecular changes at the apical membrane of epithelial cells to facilitate tube elongation.

Original languageEnglish (US)
Pages (from-to)278-288
Number of pages11
JournalDevelopmental Biology
Volume320
Issue number1
DOIs
StatePublished - Aug 1 2008

Fingerprint

Salivary Glands
Membranes
Trachea
Monomeric GTP-Binding Proteins
Cellular Structures
Nuclear Proteins
Cytoskeleton
Drosophila
Up-Regulation
Down-Regulation
Epithelial Cells
Maintenance
moesin
Proteins
BTB-POZ Domain

Keywords

  • Apical membrane
  • Crumbs
  • Lola Like
  • Moesin
  • Rab11
  • Ribbon
  • Tube morphogenesis

ASJC Scopus subject areas

  • Developmental Biology

Cite this

Ribbon modulates apical membrane during tube elongation through Crumbs and Moesin. / Kerman, Bilal E.; Cheshire, Alan M.; Myat, Monn Monn; Andrew, Deborah J.

In: Developmental Biology, Vol. 320, No. 1, 01.08.2008, p. 278-288.

Research output: Contribution to journalArticle

Kerman, Bilal E. ; Cheshire, Alan M. ; Myat, Monn Monn ; Andrew, Deborah J. / Ribbon modulates apical membrane during tube elongation through Crumbs and Moesin. In: Developmental Biology. 2008 ; Vol. 320, No. 1. pp. 278-288.
@article{d8c35969847f482a9ee539f028aa2618,
title = "Ribbon modulates apical membrane during tube elongation through Crumbs and Moesin",
abstract = "Although the formation and maintenance of epithelial tubes are essential for the viability of multicellular organisms, our understanding of the molecular and cellular events coordinating tubulogenesis is relatively limited. Here, we focus on the activities of Ribbon, a novel BTB-domain containing nuclear protein, in the elongation of two epithelial tubes: the Drosophila salivary gland and trachea. We show that Ribbon interacts with Lola Like, another BTB-domain containing protein required for robust nuclear localization of Ribbon, to upregulate crumbs expression and downregulate Moesin activity. Our ultrastructural analysis of ribbon null salivary glands by TEM reveals a diminished pool of subapical vesicles and an increase in microvillar structure, cellular changes consistent with the known role of Crumbs in apical membrane generation and of Moesin in the cross-linking of the apical membrane to the subapical cytoskeleton. Furthermore, the subapical localization of Rab11, a small GTPase associated with apical membrane delivery and rearrangement, is significantly diminished in ribbon mutant salivary glands and tracheae. These findings suggest that Ribbon and Lola Like function as a novel transcriptional cassette coordinating molecular changes at the apical membrane of epithelial cells to facilitate tube elongation.",
keywords = "Apical membrane, Crumbs, Lola Like, Moesin, Rab11, Ribbon, Tube morphogenesis",
author = "Kerman, {Bilal E.} and Cheshire, {Alan M.} and Myat, {Monn Monn} and Andrew, {Deborah J}",
year = "2008",
month = "8",
day = "1",
doi = "10.1016/j.ydbio.2008.05.541",
language = "English (US)",
volume = "320",
pages = "278--288",
journal = "Developmental Biology",
issn = "0012-1606",
publisher = "Academic Press Inc.",
number = "1",

}

TY - JOUR

T1 - Ribbon modulates apical membrane during tube elongation through Crumbs and Moesin

AU - Kerman, Bilal E.

AU - Cheshire, Alan M.

AU - Myat, Monn Monn

AU - Andrew, Deborah J

PY - 2008/8/1

Y1 - 2008/8/1

N2 - Although the formation and maintenance of epithelial tubes are essential for the viability of multicellular organisms, our understanding of the molecular and cellular events coordinating tubulogenesis is relatively limited. Here, we focus on the activities of Ribbon, a novel BTB-domain containing nuclear protein, in the elongation of two epithelial tubes: the Drosophila salivary gland and trachea. We show that Ribbon interacts with Lola Like, another BTB-domain containing protein required for robust nuclear localization of Ribbon, to upregulate crumbs expression and downregulate Moesin activity. Our ultrastructural analysis of ribbon null salivary glands by TEM reveals a diminished pool of subapical vesicles and an increase in microvillar structure, cellular changes consistent with the known role of Crumbs in apical membrane generation and of Moesin in the cross-linking of the apical membrane to the subapical cytoskeleton. Furthermore, the subapical localization of Rab11, a small GTPase associated with apical membrane delivery and rearrangement, is significantly diminished in ribbon mutant salivary glands and tracheae. These findings suggest that Ribbon and Lola Like function as a novel transcriptional cassette coordinating molecular changes at the apical membrane of epithelial cells to facilitate tube elongation.

AB - Although the formation and maintenance of epithelial tubes are essential for the viability of multicellular organisms, our understanding of the molecular and cellular events coordinating tubulogenesis is relatively limited. Here, we focus on the activities of Ribbon, a novel BTB-domain containing nuclear protein, in the elongation of two epithelial tubes: the Drosophila salivary gland and trachea. We show that Ribbon interacts with Lola Like, another BTB-domain containing protein required for robust nuclear localization of Ribbon, to upregulate crumbs expression and downregulate Moesin activity. Our ultrastructural analysis of ribbon null salivary glands by TEM reveals a diminished pool of subapical vesicles and an increase in microvillar structure, cellular changes consistent with the known role of Crumbs in apical membrane generation and of Moesin in the cross-linking of the apical membrane to the subapical cytoskeleton. Furthermore, the subapical localization of Rab11, a small GTPase associated with apical membrane delivery and rearrangement, is significantly diminished in ribbon mutant salivary glands and tracheae. These findings suggest that Ribbon and Lola Like function as a novel transcriptional cassette coordinating molecular changes at the apical membrane of epithelial cells to facilitate tube elongation.

KW - Apical membrane

KW - Crumbs

KW - Lola Like

KW - Moesin

KW - Rab11

KW - Ribbon

KW - Tube morphogenesis

UR - http://www.scopus.com/inward/record.url?scp=48949115131&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=48949115131&partnerID=8YFLogxK

U2 - 10.1016/j.ydbio.2008.05.541

DO - 10.1016/j.ydbio.2008.05.541

M3 - Article

C2 - 18585700

AN - SCOPUS:48949115131

VL - 320

SP - 278

EP - 288

JO - Developmental Biology

JF - Developmental Biology

SN - 0012-1606

IS - 1

ER -