Netrin-guided accessory cell morphogenesis dictates the dendrite orientation and migration of a Drosophila sensory neuron

Eli M. Mrkusich, Zalina B. Osman, Karen E. Bates, Julia M. Marchingo, Molly Scheel, Paul M. Whitington

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Accessory cells, which include glia and other cell types that develop in close association with neurons, have been shown to play key roles in regulating neuron development. However, the underlying molecular and cellular mechanisms remain poorly understood. A particularly intimate association between accessory cells and neurons is found in insect chordotonal organs. We have found that the cap cell, one of two accessory cells of v'ch1, a chordotonal organ in the Drosophila embryo, strongly influences the development of its associated neuron. As it projects a long dorsally directed cellular extension, the cap cell reorients the dendrite of the v'ch1 neuron and tows its cell body dorsally. Cap cell morphogenesis is regulated by Netrin-A, which is produced by epidermal cells at the destination of the cap cell process. In Netrin-A mutant embryos, the cap cell forms an aberrant, ventrally directed process. As the cap cell maintains a close physical connection with the tip of the dendrite, the latter is dragged into an abnormal position and orientation, and the neuron fails to undergo its normal dorsal migration. Misexpression of Netrin-A in oenocytes, secretory cells that lie ventral to the cap cell, leads to aberrant cap cell morphogenesis, suggesting that Netrin-A acts as an instructive cue to direct the growth of the cap cell process. The netrin receptor Frazzled is required for normal cap cell morphogenesis, and mutant rescue experiments indicate that it acts in a cell-autonomous fashion.

Original languageEnglish
Pages (from-to)2227-2235
Number of pages9
JournalDevelopment (Cambridge)
Volume137
Issue number13
DOIs
StatePublished - Jul 1 2010

Fingerprint

Sensory Receptor Cells
Dendrites
Morphogenesis
Drosophila
Neurons
Cell Growth Processes
Embryonic Structures
Neuroglia
Cues
Insects

Keywords

  • Cap cell
  • Chordotonal organ
  • Dendrite growth
  • Drosophila
  • Frazzled
  • Netrin
  • Neuron migration

ASJC Scopus subject areas

  • Developmental Biology
  • Molecular Biology

Cite this

Netrin-guided accessory cell morphogenesis dictates the dendrite orientation and migration of a Drosophila sensory neuron. / Mrkusich, Eli M.; Osman, Zalina B.; Bates, Karen E.; Marchingo, Julia M.; Scheel, Molly; Whitington, Paul M.

In: Development (Cambridge), Vol. 137, No. 13, 01.07.2010, p. 2227-2235.

Research output: Contribution to journalArticle

Mrkusich, Eli M. ; Osman, Zalina B. ; Bates, Karen E. ; Marchingo, Julia M. ; Scheel, Molly ; Whitington, Paul M. / Netrin-guided accessory cell morphogenesis dictates the dendrite orientation and migration of a Drosophila sensory neuron. In: Development (Cambridge). 2010 ; Vol. 137, No. 13. pp. 2227-2235.
@article{69ea9b285224438baefbdae577c76527,
title = "Netrin-guided accessory cell morphogenesis dictates the dendrite orientation and migration of a Drosophila sensory neuron",
abstract = "Accessory cells, which include glia and other cell types that develop in close association with neurons, have been shown to play key roles in regulating neuron development. However, the underlying molecular and cellular mechanisms remain poorly understood. A particularly intimate association between accessory cells and neurons is found in insect chordotonal organs. We have found that the cap cell, one of two accessory cells of v'ch1, a chordotonal organ in the Drosophila embryo, strongly influences the development of its associated neuron. As it projects a long dorsally directed cellular extension, the cap cell reorients the dendrite of the v'ch1 neuron and tows its cell body dorsally. Cap cell morphogenesis is regulated by Netrin-A, which is produced by epidermal cells at the destination of the cap cell process. In Netrin-A mutant embryos, the cap cell forms an aberrant, ventrally directed process. As the cap cell maintains a close physical connection with the tip of the dendrite, the latter is dragged into an abnormal position and orientation, and the neuron fails to undergo its normal dorsal migration. Misexpression of Netrin-A in oenocytes, secretory cells that lie ventral to the cap cell, leads to aberrant cap cell morphogenesis, suggesting that Netrin-A acts as an instructive cue to direct the growth of the cap cell process. The netrin receptor Frazzled is required for normal cap cell morphogenesis, and mutant rescue experiments indicate that it acts in a cell-autonomous fashion.",
keywords = "Cap cell, Chordotonal organ, Dendrite growth, Drosophila, Frazzled, Netrin, Neuron migration",
author = "Mrkusich, {Eli M.} and Osman, {Zalina B.} and Bates, {Karen E.} and Marchingo, {Julia M.} and Molly Scheel and Whitington, {Paul M.}",
year = "2010",
month = "7",
day = "1",
doi = "10.1242/dev.047795",
language = "English",
volume = "137",
pages = "2227--2235",
journal = "Development",
issn = "0950-1991",
publisher = "Company of Biologists Ltd",
number = "13",

}

TY - JOUR

T1 - Netrin-guided accessory cell morphogenesis dictates the dendrite orientation and migration of a Drosophila sensory neuron

AU - Mrkusich, Eli M.

AU - Osman, Zalina B.

AU - Bates, Karen E.

AU - Marchingo, Julia M.

AU - Scheel, Molly

AU - Whitington, Paul M.

PY - 2010/7/1

Y1 - 2010/7/1

N2 - Accessory cells, which include glia and other cell types that develop in close association with neurons, have been shown to play key roles in regulating neuron development. However, the underlying molecular and cellular mechanisms remain poorly understood. A particularly intimate association between accessory cells and neurons is found in insect chordotonal organs. We have found that the cap cell, one of two accessory cells of v'ch1, a chordotonal organ in the Drosophila embryo, strongly influences the development of its associated neuron. As it projects a long dorsally directed cellular extension, the cap cell reorients the dendrite of the v'ch1 neuron and tows its cell body dorsally. Cap cell morphogenesis is regulated by Netrin-A, which is produced by epidermal cells at the destination of the cap cell process. In Netrin-A mutant embryos, the cap cell forms an aberrant, ventrally directed process. As the cap cell maintains a close physical connection with the tip of the dendrite, the latter is dragged into an abnormal position and orientation, and the neuron fails to undergo its normal dorsal migration. Misexpression of Netrin-A in oenocytes, secretory cells that lie ventral to the cap cell, leads to aberrant cap cell morphogenesis, suggesting that Netrin-A acts as an instructive cue to direct the growth of the cap cell process. The netrin receptor Frazzled is required for normal cap cell morphogenesis, and mutant rescue experiments indicate that it acts in a cell-autonomous fashion.

AB - Accessory cells, which include glia and other cell types that develop in close association with neurons, have been shown to play key roles in regulating neuron development. However, the underlying molecular and cellular mechanisms remain poorly understood. A particularly intimate association between accessory cells and neurons is found in insect chordotonal organs. We have found that the cap cell, one of two accessory cells of v'ch1, a chordotonal organ in the Drosophila embryo, strongly influences the development of its associated neuron. As it projects a long dorsally directed cellular extension, the cap cell reorients the dendrite of the v'ch1 neuron and tows its cell body dorsally. Cap cell morphogenesis is regulated by Netrin-A, which is produced by epidermal cells at the destination of the cap cell process. In Netrin-A mutant embryos, the cap cell forms an aberrant, ventrally directed process. As the cap cell maintains a close physical connection with the tip of the dendrite, the latter is dragged into an abnormal position and orientation, and the neuron fails to undergo its normal dorsal migration. Misexpression of Netrin-A in oenocytes, secretory cells that lie ventral to the cap cell, leads to aberrant cap cell morphogenesis, suggesting that Netrin-A acts as an instructive cue to direct the growth of the cap cell process. The netrin receptor Frazzled is required for normal cap cell morphogenesis, and mutant rescue experiments indicate that it acts in a cell-autonomous fashion.

KW - Cap cell

KW - Chordotonal organ

KW - Dendrite growth

KW - Drosophila

KW - Frazzled

KW - Netrin

KW - Neuron migration

UR - http://www.scopus.com/inward/record.url?scp=77953304433&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=77953304433&partnerID=8YFLogxK

U2 - 10.1242/dev.047795

DO - 10.1242/dev.047795

M3 - Article

C2 - 20530550

AN - SCOPUS:77953304433

VL - 137

SP - 2227

EP - 2235

JO - Development

JF - Development

SN - 0950-1991

IS - 13

ER -