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The Journal of Neuroscience, April 1, 2009, 29(13):4065-4075; doi:10.1523/JNEUROSCI.0044-09.2009

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Cellular/Molecular
Intraflagellar Transport/Hedgehog-Related Signaling Components Couple Sensory Cilium Morphology and Serotonin Biosynthesis in Caenorhabditis elegans

Mustapha Moussaif and Ji Ying Sze

Department of Molecular Pharmacology, Albert Einstein College of Medicine, Bronx, New York 10461

Correspondence should be addressed to Ji Ying Sze, Department of Molecular Pharmacology, Albert Einstein College of Medicine, 202 Golding Building, 1300 Morris Park Avenue, Bronx, NY 10461. Email: jsze{at}aecom.yu.edu

Intraflagellar transport in cilia has been proposed as a crucial mediator of Hedgehog signal transduction during embryonic pattern formation in both vertebrates and invertebrates. Here, we show that the Hh receptor Patched-related factor DAF-6 and intraflagellar transport modulate serotonin production in Caenorhabditis elegans animals, by remodeling the architecture of dendritic cilia of a pair of ADF serotonergic chemosensory neurons. Wild-type animals under aversive environment drastically reduce DAF-6 expression in glia-like cells surrounding the cilia of chemosensory neurons, resulting in cilium structural remodeling and upregulation of the serotonin-biosynthesis enzyme tryptophan hydroxylase tph-1 in the ADF neurons. These cellular and molecular modifications are reversed when the environment improves. Mutants of daf-6 or intraflagellar transport constitutively upregulate tph-1 expression. Epistasis analyses indicate that DAF-6/intraflagellar transport and the OCR-2/OSM-9 TRPV channel act in concert, regulating two layers of activation of tph-1 in the ADF neurons. The TRPV signaling turns on tph-1 expression under favorable and aversive conditions, whereas inactivation of DAF-6 by stress results in further upregulation of tph-1 independently of OCR-2/OSM-9 activity. Behavioral analyses suggest that serotonin facilitates larval animals resuming development when the environment improves. Our study revealed the cilium structure of serotonergic neurons as a trigger of regulated serotonin production, and demonstrated that a Hedgehog-related signaling component is dynamically regulated by environment and underscores neuroplasticity of serotonergic neurons in C. elegans under stress and stress recovery.

Received Jan. 5, 2009; revised Feb. 19, 2009; accepted Feb. 19, 2009.

Correspondence should be addressed to Ji Ying Sze, Department of Molecular Pharmacology, Albert Einstein College of Medicine, 202 Golding Building, 1300 Morris Park Avenue, Bronx, NY 10461. Email: jsze{at}aecom.yu.edu






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