Neuronal serotonin release triggers the heat shock response in C. elegans in the absence of temperature increase

Marcus C Tatum; Felicia K Ooi; Madhusudana Rao Chikka; Laetitia Chauve; Luis A Martinez-Velazquez; Harry W M Steinbusch; Richard I Morimoto; Veena Prahlad

doi:10.1016/j.cub.2014.11.040

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Neuronal serotonin release triggers the heat shock response in C. elegans in the absence of temperature increase

Journal article

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Neuronal serotonin release triggers the heat shock response in C. elegans in the absence of temperature increase

Marcus C Tatum, Felicia K Ooi, Madhusudana Rao Chikka, Laetitia Chauve, Luis A Martinez-Velazquez, Harry W M Steinbusch, Richard I Morimoto and Veena Prahlad

Current biology, Vol.25(2), pp.163-174

01/19/2015

DOI: 10.1016/j.cub.2014.11.040

PMCID: PMC4840938

PMID: 25557666

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Abstract

Cellular mechanisms aimed at repairing protein damage and maintaining homeostasis, widely understood to be triggered by the damage itself, have recently been shown to be under cell nonautonomous control in the metazoan C. elegans. The heat shock response (HSR) is one such conserved mechanism, activated by cells upon exposure to proteotoxic conditions such as heat. Previously, we had shown that this conserved cytoprotective response is regulated by the thermosensory neuronal circuitry of C. elegans. Here, we investigate the mechanisms and physiological relevance of neuronal control. By combining optogenetic methods with live visualization of the dynamics of the heat shock transcription factor (HSF1), we show that excitation of the AFD thermosensory neurons is sufficient to activate HSF1 in another cell, even in the absence of temperature increase. Excitation of the AFD thermosensory neurons enhances serotonin release. Serotonin release elicited by direct optogenetic stimulation of serotonergic neurons activates HSF1 and upregulates molecular chaperones through the metabotropic serotonin receptor SER-1. Consequently, excitation of serotonergic neurons alone can suppress protein misfolding in C. elegans peripheral tissue. These studies imply that thermosensory activity coupled to serotonergic signaling is sufficient to activate the protective HSR prior to frank proteotoxic damage. The ability of neurosensory release of serotonin to control cellular stress responses and activate HSF1 has powerful implications for the treatment of protein conformation diseases.

Transcription Factors - metabolism

Caenorhabditis elegans - physiology

Heat-Shock Response

Temperature

Animals

Caenorhabditis elegans - genetics

Serotonin - metabolism

Gene Expression Regulation

Caenorhabditis elegans Proteins - metabolism

Transcription Factors - genetics

Reverse Transcriptase Polymerase Chain Reaction

Caenorhabditis elegans Proteins - genetics

Details

Title: Subtitle: Neuronal serotonin release triggers the heat shock response in C. elegans in the absence of temperature increase
Creators: Marcus C Tatum - Department of Biology, Aging Mind and Brain Initiative, University of Iowa, 338 Biology Building East, 210 Iowa Avenue, Iowa City, IA 52242-1324, USA
Felicia K Ooi - Department of Biology, Aging Mind and Brain Initiative, University of Iowa, 338 Biology Building East, 210 Iowa Avenue, Iowa City, IA 52242-1324, USA
Madhusudana Rao Chikka - Department of Biology, Aging Mind and Brain Initiative, University of Iowa, 338 Biology Building East, 210 Iowa Avenue, Iowa City, IA 52242-1324, USA
Laetitia Chauve - Department of Molecular Biosciences, Rice Institute for Biomedical Sciences, Northwestern University, 2205 Tech Drive, Hogan 2-100, Evanston, IL 60208-3500, USA
Luis A Martinez-Velazquez - Program in Cellular Neuroscience, Neurodegeneration, and Repair, Department of Cell Biology, Yale University School of Medicine, 333 Cedar Street, P.O. Box 208002, New Haven, CT 06520-8002, USA
Harry W M Steinbusch - Department Translational Neuroscience, Faculty of Health, Medicine and Life Sciences, Maastricht University Medical Center, Universiteitssingel 40, Room 2.578, P.O. Box 616, 6200 MD Maastricht, the Netherlands
Richard I Morimoto - Department of Molecular Biosciences, Rice Institute for Biomedical Sciences, Northwestern University, 2205 Tech Drive, Hogan 2-100, Evanston, IL 60208-3500, USA
Veena Prahlad - Department of Biology, Aging Mind and Brain Initiative, University of Iowa, 338 Biology Building East, 210 Iowa Avenue, Iowa City, IA 52242-1324, USA. Electronic address: veena-prahlad@uiowa.edu
Resource Type: Journal article
Publication Details: Current biology, Vol.25(2), pp.163-174
Publisher: England
DOI: 10.1016/j.cub.2014.11.040
PMID: 25557666
PMCID: PMC4840938
ISSN: 0960-9822
eISSN: 1879-0445
Grant note: R01 AG026647 / NIA NIH HHS R21 NS056337 / NINDS NIH HHS R00 NS057931 / NINDS NIH HHS K99 NS057931 / NINDS NIH HHS R37 AG026647 / NIA NIH HHS R01 GM038109 / NIGMS NIH HHS P40 OD010440 / NIH HHS NS057931 / NINDS NIH HHS
Language: English
Date published: 01/19/2015
Academic Unit: Iowa Neuroscience Institute; Biology; Industrial and Systems Engineering
Record Identifier: 9983991999502771

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