Unique and overlapping functions of formins frl and DAAM during ommatidial rotation and neuronal development in Drosophila

Gretchen Dollar, Rita Gombos, Austen A. Barnett, David Sanchez Hernandez, Saw M T Maung, Jozsef Mihály, Andreas Jenny

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

The noncanonical Frizzled/planar cell polarity (PCP) pathway regulates establishment of polarity within the plane of an epithelium to generate diversity of cell fates, asymmetric, but highly aligned structures, or to orchestrate the directional migration of cells during convergent extension during vertebrate gastrulation. In Drosophila, PCP signaling is essential to orient actin wing hairs and to align ommatidia in the eye, in part by coordinating the movement of groups of photoreceptor cells during ommatidial rotation. Importantly, the coordination of PCP signaling with changes in the cytoskeleton is essential for proper epithelial polarity. Formins polymerize linear actin filaments and are key regulators of the actin cytoskeleton. Here, we show that the diaphanous-related formin, Frl, the single fly member of the FMNL (formin related in leukocytes/formin-like) formin subfamily affects ommatidial rotation in the Drosophila eye and is controlled by the Rho family GTPase Cdc42. Interestingly, we also found that frl mutants exhibit an axon growth phenotype in the mushroom body, a center for olfactory learning in the Drosophila brain, which is also affected in a subset of PCP genes. Significantly, Frl cooperates with Cdc42 and another formin, DAAM, during mushroom body formation. This study thus suggests that different formins can cooperate or act independently in distinct tissues, likely integrating various signaling inputs with the regulation of the cytoskeleton. It furthermore highlights the importance and complexity of formin-dependent cytoskeletal regulation in multiple organs and developmental contexts. planar cell polarity; formin; cytoskeleton; neural development; noncanonical Wnt signaling.

Original languageEnglish (US)
Pages (from-to)1135-1151
Number of pages17
JournalGenetics
Volume202
Issue number3
DOIs
StatePublished - Mar 1 2016

Fingerprint

Cell Polarity
Drosophila
Cytoskeleton
Mushroom Bodies
Actin Cytoskeleton
rho GTP-Binding Proteins
Gastrulation
Photoreceptor Cells
Diptera
Cell Movement
Axons
Vertebrates
Actins
Leukocytes
Epithelium
Learning
Phenotype
Brain
Growth
Genes

ASJC Scopus subject areas

  • Genetics

Cite this

Unique and overlapping functions of formins frl and DAAM during ommatidial rotation and neuronal development in Drosophila. / Dollar, Gretchen; Gombos, Rita; Barnett, Austen A.; Hernandez, David Sanchez; Maung, Saw M T; Mihály, Jozsef; Jenny, Andreas.

In: Genetics, Vol. 202, No. 3, 01.03.2016, p. 1135-1151.

Research output: Contribution to journalArticle

Dollar, Gretchen ; Gombos, Rita ; Barnett, Austen A. ; Hernandez, David Sanchez ; Maung, Saw M T ; Mihály, Jozsef ; Jenny, Andreas. / Unique and overlapping functions of formins frl and DAAM during ommatidial rotation and neuronal development in Drosophila. In: Genetics. 2016 ; Vol. 202, No. 3. pp. 1135-1151.
@article{da7db413cee0476b9cca539b22a69a88,
title = "Unique and overlapping functions of formins frl and DAAM during ommatidial rotation and neuronal development in Drosophila",
abstract = "The noncanonical Frizzled/planar cell polarity (PCP) pathway regulates establishment of polarity within the plane of an epithelium to generate diversity of cell fates, asymmetric, but highly aligned structures, or to orchestrate the directional migration of cells during convergent extension during vertebrate gastrulation. In Drosophila, PCP signaling is essential to orient actin wing hairs and to align ommatidia in the eye, in part by coordinating the movement of groups of photoreceptor cells during ommatidial rotation. Importantly, the coordination of PCP signaling with changes in the cytoskeleton is essential for proper epithelial polarity. Formins polymerize linear actin filaments and are key regulators of the actin cytoskeleton. Here, we show that the diaphanous-related formin, Frl, the single fly member of the FMNL (formin related in leukocytes/formin-like) formin subfamily affects ommatidial rotation in the Drosophila eye and is controlled by the Rho family GTPase Cdc42. Interestingly, we also found that frl mutants exhibit an axon growth phenotype in the mushroom body, a center for olfactory learning in the Drosophila brain, which is also affected in a subset of PCP genes. Significantly, Frl cooperates with Cdc42 and another formin, DAAM, during mushroom body formation. This study thus suggests that different formins can cooperate or act independently in distinct tissues, likely integrating various signaling inputs with the regulation of the cytoskeleton. It furthermore highlights the importance and complexity of formin-dependent cytoskeletal regulation in multiple organs and developmental contexts. planar cell polarity; formin; cytoskeleton; neural development; noncanonical Wnt signaling.",
author = "Gretchen Dollar and Rita Gombos and Barnett, {Austen A.} and Hernandez, {David Sanchez} and Maung, {Saw M T} and Jozsef Mih{\'a}ly and Andreas Jenny",
year = "2016",
month = "3",
day = "1",
doi = "10.1534/genetics.115.181438",
language = "English (US)",
volume = "202",
pages = "1135--1151",
journal = "Genetics",
issn = "0016-6731",
publisher = "Genetics Society of America",
number = "3",

}

TY - JOUR

T1 - Unique and overlapping functions of formins frl and DAAM during ommatidial rotation and neuronal development in Drosophila

AU - Dollar, Gretchen

AU - Gombos, Rita

AU - Barnett, Austen A.

AU - Hernandez, David Sanchez

AU - Maung, Saw M T

AU - Mihály, Jozsef

AU - Jenny, Andreas

PY - 2016/3/1

Y1 - 2016/3/1

N2 - The noncanonical Frizzled/planar cell polarity (PCP) pathway regulates establishment of polarity within the plane of an epithelium to generate diversity of cell fates, asymmetric, but highly aligned structures, or to orchestrate the directional migration of cells during convergent extension during vertebrate gastrulation. In Drosophila, PCP signaling is essential to orient actin wing hairs and to align ommatidia in the eye, in part by coordinating the movement of groups of photoreceptor cells during ommatidial rotation. Importantly, the coordination of PCP signaling with changes in the cytoskeleton is essential for proper epithelial polarity. Formins polymerize linear actin filaments and are key regulators of the actin cytoskeleton. Here, we show that the diaphanous-related formin, Frl, the single fly member of the FMNL (formin related in leukocytes/formin-like) formin subfamily affects ommatidial rotation in the Drosophila eye and is controlled by the Rho family GTPase Cdc42. Interestingly, we also found that frl mutants exhibit an axon growth phenotype in the mushroom body, a center for olfactory learning in the Drosophila brain, which is also affected in a subset of PCP genes. Significantly, Frl cooperates with Cdc42 and another formin, DAAM, during mushroom body formation. This study thus suggests that different formins can cooperate or act independently in distinct tissues, likely integrating various signaling inputs with the regulation of the cytoskeleton. It furthermore highlights the importance and complexity of formin-dependent cytoskeletal regulation in multiple organs and developmental contexts. planar cell polarity; formin; cytoskeleton; neural development; noncanonical Wnt signaling.

AB - The noncanonical Frizzled/planar cell polarity (PCP) pathway regulates establishment of polarity within the plane of an epithelium to generate diversity of cell fates, asymmetric, but highly aligned structures, or to orchestrate the directional migration of cells during convergent extension during vertebrate gastrulation. In Drosophila, PCP signaling is essential to orient actin wing hairs and to align ommatidia in the eye, in part by coordinating the movement of groups of photoreceptor cells during ommatidial rotation. Importantly, the coordination of PCP signaling with changes in the cytoskeleton is essential for proper epithelial polarity. Formins polymerize linear actin filaments and are key regulators of the actin cytoskeleton. Here, we show that the diaphanous-related formin, Frl, the single fly member of the FMNL (formin related in leukocytes/formin-like) formin subfamily affects ommatidial rotation in the Drosophila eye and is controlled by the Rho family GTPase Cdc42. Interestingly, we also found that frl mutants exhibit an axon growth phenotype in the mushroom body, a center for olfactory learning in the Drosophila brain, which is also affected in a subset of PCP genes. Significantly, Frl cooperates with Cdc42 and another formin, DAAM, during mushroom body formation. This study thus suggests that different formins can cooperate or act independently in distinct tissues, likely integrating various signaling inputs with the regulation of the cytoskeleton. It furthermore highlights the importance and complexity of formin-dependent cytoskeletal regulation in multiple organs and developmental contexts. planar cell polarity; formin; cytoskeleton; neural development; noncanonical Wnt signaling.

UR - http://www.scopus.com/inward/record.url?scp=84979941656&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84979941656&partnerID=8YFLogxK

U2 - 10.1534/genetics.115.181438

DO - 10.1534/genetics.115.181438

M3 - Article

C2 - 26801180

AN - SCOPUS:84979941656

VL - 202

SP - 1135

EP - 1151

JO - Genetics

JF - Genetics

SN - 0016-6731

IS - 3

ER -