Sensory Signaling-Dependent Remodeling of Olfactory Cilia Architecture in C. elegans

Saikat Mukhopadhyay, Yun Lu, Shai Shaham, Piali Sengupta

Research output: Contribution to journalArticle

78 Citations (Scopus)

Abstract

Nonmotile primary cilia are sensory organelles composed of a microtubular axoneme and a surrounding membrane sheath that houses signaling molecules. Optimal cellular function requires the precise regulation of axoneme assembly, membrane biogenesis, and signaling protein targeting and localization via as yet poorly understood mechanisms. Here, we show that sensory signaling is required to maintain the architecture of the specialized AWB olfactory neuron cilia in C. elegans. Decreased sensory signaling results in alteration of axoneme length and expansion of a membraneous structure, thereby altering the topological distribution of a subset of ciliary transmembrane signaling molecules. Signaling-regulated alteration of ciliary structures can be bypassed by modulation of intracellular cGMP or calcium levels and requires kinesin-II-driven intraflagellar transport (IFT), as well as BBS- and RAB8-related proteins. Our results suggest that compensatory mechanisms in response to altered levels of sensory activity modulate AWB cilia architecture, revealing remarkable plasticity in the regulation of cilia structure.

Original languageEnglish (US)
Pages (from-to)762-774
Number of pages13
JournalDevelopmental Cell
Volume14
Issue number5
DOIs
StatePublished - May 13 2008

Fingerprint

Cilia
Axoneme
Membranes
Protein Transport
Organelles
Bulletin boards
Molecules
Calcium
Neurons
Plasticity
Proteins
Modulation

Keywords

  • DEVBIO
  • SIGNALING

ASJC Scopus subject areas

  • Developmental Biology

Cite this

Sensory Signaling-Dependent Remodeling of Olfactory Cilia Architecture in C. elegans. / Mukhopadhyay, Saikat; Lu, Yun; Shaham, Shai; Sengupta, Piali.

In: Developmental Cell, Vol. 14, No. 5, 13.05.2008, p. 762-774.

Research output: Contribution to journalArticle

Mukhopadhyay, Saikat ; Lu, Yun ; Shaham, Shai ; Sengupta, Piali. / Sensory Signaling-Dependent Remodeling of Olfactory Cilia Architecture in C. elegans. In: Developmental Cell. 2008 ; Vol. 14, No. 5. pp. 762-774.
@article{44784605093d45a1bbbcbfd0b99ebcbd,
title = "Sensory Signaling-Dependent Remodeling of Olfactory Cilia Architecture in C. elegans",
abstract = "Nonmotile primary cilia are sensory organelles composed of a microtubular axoneme and a surrounding membrane sheath that houses signaling molecules. Optimal cellular function requires the precise regulation of axoneme assembly, membrane biogenesis, and signaling protein targeting and localization via as yet poorly understood mechanisms. Here, we show that sensory signaling is required to maintain the architecture of the specialized AWB olfactory neuron cilia in C. elegans. Decreased sensory signaling results in alteration of axoneme length and expansion of a membraneous structure, thereby altering the topological distribution of a subset of ciliary transmembrane signaling molecules. Signaling-regulated alteration of ciliary structures can be bypassed by modulation of intracellular cGMP or calcium levels and requires kinesin-II-driven intraflagellar transport (IFT), as well as BBS- and RAB8-related proteins. Our results suggest that compensatory mechanisms in response to altered levels of sensory activity modulate AWB cilia architecture, revealing remarkable plasticity in the regulation of cilia structure.",
keywords = "DEVBIO, SIGNALING",
author = "Saikat Mukhopadhyay and Yun Lu and Shai Shaham and Piali Sengupta",
year = "2008",
month = "5",
day = "13",
doi = "10.1016/j.devcel.2008.03.002",
language = "English (US)",
volume = "14",
pages = "762--774",
journal = "Developmental Cell",
issn = "1534-5807",
publisher = "Cell Press",
number = "5",

}

TY - JOUR

T1 - Sensory Signaling-Dependent Remodeling of Olfactory Cilia Architecture in C. elegans

AU - Mukhopadhyay, Saikat

AU - Lu, Yun

AU - Shaham, Shai

AU - Sengupta, Piali

PY - 2008/5/13

Y1 - 2008/5/13

N2 - Nonmotile primary cilia are sensory organelles composed of a microtubular axoneme and a surrounding membrane sheath that houses signaling molecules. Optimal cellular function requires the precise regulation of axoneme assembly, membrane biogenesis, and signaling protein targeting and localization via as yet poorly understood mechanisms. Here, we show that sensory signaling is required to maintain the architecture of the specialized AWB olfactory neuron cilia in C. elegans. Decreased sensory signaling results in alteration of axoneme length and expansion of a membraneous structure, thereby altering the topological distribution of a subset of ciliary transmembrane signaling molecules. Signaling-regulated alteration of ciliary structures can be bypassed by modulation of intracellular cGMP or calcium levels and requires kinesin-II-driven intraflagellar transport (IFT), as well as BBS- and RAB8-related proteins. Our results suggest that compensatory mechanisms in response to altered levels of sensory activity modulate AWB cilia architecture, revealing remarkable plasticity in the regulation of cilia structure.

AB - Nonmotile primary cilia are sensory organelles composed of a microtubular axoneme and a surrounding membrane sheath that houses signaling molecules. Optimal cellular function requires the precise regulation of axoneme assembly, membrane biogenesis, and signaling protein targeting and localization via as yet poorly understood mechanisms. Here, we show that sensory signaling is required to maintain the architecture of the specialized AWB olfactory neuron cilia in C. elegans. Decreased sensory signaling results in alteration of axoneme length and expansion of a membraneous structure, thereby altering the topological distribution of a subset of ciliary transmembrane signaling molecules. Signaling-regulated alteration of ciliary structures can be bypassed by modulation of intracellular cGMP or calcium levels and requires kinesin-II-driven intraflagellar transport (IFT), as well as BBS- and RAB8-related proteins. Our results suggest that compensatory mechanisms in response to altered levels of sensory activity modulate AWB cilia architecture, revealing remarkable plasticity in the regulation of cilia structure.

KW - DEVBIO

KW - SIGNALING

UR - http://www.scopus.com/inward/record.url?scp=43049129288&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=43049129288&partnerID=8YFLogxK

U2 - 10.1016/j.devcel.2008.03.002

DO - 10.1016/j.devcel.2008.03.002

M3 - Article

VL - 14

SP - 762

EP - 774

JO - Developmental Cell

JF - Developmental Cell

SN - 1534-5807

IS - 5

ER -