An Afferent Neuropeptide System Transmits Mechanosensory Signals Triggering Sensitization and Arousal in C. elegans

Yee Lian Chew; Yoshinori Tanizawa; Yongmin Cho; Buyun Zhao; Alex J. Yu; Evan L. Ardiel; Ithai Rabinowitch; Jihong Bai; Catharine H. Rankin; Hang Lu; Isabel Beets; William R. Schafer

doi:10.1016/j.neuron.2018.08.003

An Afferent Neuropeptide System Transmits Mechanosensory Signals Triggering Sensitization and Arousal in C. elegans

Yee Lian Chew, Yoshinori Tanizawa, Yongmin Cho, Buyun Zhao, Alex J. Yu, Evan L. Ardiel, Ithai Rabinowitch, Jihong Bai, Catharine H. Rankin, Hang Lu, Isabel Beets, William R. Schafer^*

^*Corresponding author for this work

Department of Medical Neurobiology

Research output: Contribution to journal › Article › peer-review

31 Scopus citations

Abstract

Sensitization is a simple form of behavioral plasticity by which an initial stimulus, often signaling danger, leads to increased responsiveness to subsequent stimuli. Cross-modal sensitization is an important feature of arousal in many organisms, yet its molecular and neural mechanisms are incompletely understood. Here we show that in C. elegans, aversive mechanical stimuli lead to both enhanced locomotor activity and sensitization of aversive chemosensory pathways. Both locomotor arousal and cross-modal sensitization depend on the release of FLP-20 neuropeptides from primary mechanosensory neurons and on their receptor FRPR-3. Surprisingly, the critical site of action of FRPR-3 for both sensory and locomotor arousal is RID, a single neuroendocrine cell specialized for the release of neuropeptides that responds to mechanical stimuli in a FLP-20-dependent manner. Thus, FLP-20 peptides function as an afferent arousal signal that conveys mechanosensory information to central neurons that modulate arousal and other behavioral states. Video Abstract:[Figure presented] Arousal is an important conserved behavioral state where animals show increased sensory responsiveness and locomotor hyperactivity. Chew et al. identify a neuromodulatory pathway that enables mechanosensory neurons to promote both sensory and locomotor arousal via activation of a neuroendocrine center.

Original language	American English
Pages (from-to)	1233-1246.e6
Journal	Neuron
Volume	99
Issue number	6
DOIs	https://doi.org/10.1016/j.neuron.2018.08.003
State	Published - 19 Sep 2018

Bibliographical note

Funding Information:
The authors gratefully acknowledge Denise Walker for critical reading of the manuscript, and members of the Schafer, de Bono, and Taylor labs (MRC LMB) and Young-Jai You (Nagoya University) for helpful discussions. We sincerely thank Inja Radman for some DNA constructs. Some strains were provided by the CGC, which is funded by the National Institutes of Health (NIH P40 OD010440 ). We are grateful to Dr. Mei Zhen for the RID::Chrimson line ZM9315. This work was funded by grants from the Medical Research Council ( MC-A023-5PB91 ) and the Wellcome Trust ( WT103784MA ) to W.R.S., from the NIH ( R21DC015652 ) to W.R.S. and H.L., from the NIH ( R01NS096581 and R01GM088333 ) to H.L., from the Natural Sciences and Engineering Research Council of Canada (NSERC grant #122216-2013 ) to C.H.R., and from the NIH ( R21DC016258 ) to J.B. Y.L.C. is funded by an EMBO Long-term Fellowship (ALTF 403-2016). A.J.Y. is funded by a NSERC Canada Graduate Scholarship-Master’s (CGS-M). E.L.A. is funded by a NSERC CGS. I.B. is funded by an EMBO Long-term Fellowship (ALTF 387-2015) and is a fellow of the Research Foundation - Flanders (FWO).

Publisher Copyright:
© 2018 MRC Laboratory of Molecular Biology

Keywords

C. elegans
arousal
behavioral states
neuropeptides
sensitization

Access to Document

10.1016/j.neuron.2018.08.003

Cite this

@article{c4ab14cadd664f52ae0cc0f95880abc1,

title = "An Afferent Neuropeptide System Transmits Mechanosensory Signals Triggering Sensitization and Arousal in C. elegans",

abstract = "Sensitization is a simple form of behavioral plasticity by which an initial stimulus, often signaling danger, leads to increased responsiveness to subsequent stimuli. Cross-modal sensitization is an important feature of arousal in many organisms, yet its molecular and neural mechanisms are incompletely understood. Here we show that in C. elegans, aversive mechanical stimuli lead to both enhanced locomotor activity and sensitization of aversive chemosensory pathways. Both locomotor arousal and cross-modal sensitization depend on the release of FLP-20 neuropeptides from primary mechanosensory neurons and on their receptor FRPR-3. Surprisingly, the critical site of action of FRPR-3 for both sensory and locomotor arousal is RID, a single neuroendocrine cell specialized for the release of neuropeptides that responds to mechanical stimuli in a FLP-20-dependent manner. Thus, FLP-20 peptides function as an afferent arousal signal that conveys mechanosensory information to central neurons that modulate arousal and other behavioral states. Video Abstract:[Figure presented] Arousal is an important conserved behavioral state where animals show increased sensory responsiveness and locomotor hyperactivity. Chew et al. identify a neuromodulatory pathway that enables mechanosensory neurons to promote both sensory and locomotor arousal via activation of a neuroendocrine center.",

keywords = "C. elegans, arousal, behavioral states, neuropeptides, sensitization",

author = "Chew, {Yee Lian} and Yoshinori Tanizawa and Yongmin Cho and Buyun Zhao and Yu, {Alex J.} and Ardiel, {Evan L.} and Ithai Rabinowitch and Jihong Bai and Rankin, {Catharine H.} and Hang Lu and Isabel Beets and Schafer, {William R.}",

note = "Funding Information: The authors gratefully acknowledge Denise Walker for critical reading of the manuscript, and members of the Schafer, de Bono, and Taylor labs (MRC LMB) and Young-Jai You (Nagoya University) for helpful discussions. We sincerely thank Inja Radman for some DNA constructs. Some strains were provided by the CGC, which is funded by the National Institutes of Health (NIH P40 OD010440 ). We are grateful to Dr. Mei Zhen for the RID::Chrimson line ZM9315. This work was funded by grants from the Medical Research Council ( MC-A023-5PB91 ) and the Wellcome Trust ( WT103784MA ) to W.R.S., from the NIH ( R21DC015652 ) to W.R.S. and H.L., from the NIH ( R01NS096581 and R01GM088333 ) to H.L., from the Natural Sciences and Engineering Research Council of Canada (NSERC grant #122216-2013 ) to C.H.R., and from the NIH ( R21DC016258 ) to J.B. Y.L.C. is funded by an EMBO Long-term Fellowship (ALTF 403-2016). A.J.Y. is funded by a NSERC Canada Graduate Scholarship-Master{\textquoteright}s (CGS-M). E.L.A. is funded by a NSERC CGS. I.B. is funded by an EMBO Long-term Fellowship (ALTF 387-2015) and is a fellow of the Research Foundation - Flanders (FWO). Publisher Copyright: {\textcopyright} 2018 MRC Laboratory of Molecular Biology",

year = "2018",

month = sep,

day = "19",

doi = "10.1016/j.neuron.2018.08.003",

language = "American English",

volume = "99",

pages = "1233--1246.e6",

journal = "Neuron",

issn = "0896-6273",

publisher = "Cell Press",

number = "6",

}

TY - JOUR

T1 - An Afferent Neuropeptide System Transmits Mechanosensory Signals Triggering Sensitization and Arousal in C. elegans

AU - Chew, Yee Lian

AU - Tanizawa, Yoshinori

AU - Cho, Yongmin

AU - Zhao, Buyun

AU - Yu, Alex J.

AU - Ardiel, Evan L.

AU - Rabinowitch, Ithai

AU - Bai, Jihong

AU - Rankin, Catharine H.

AU - Lu, Hang

AU - Beets, Isabel

AU - Schafer, William R.

N1 - Funding Information: The authors gratefully acknowledge Denise Walker for critical reading of the manuscript, and members of the Schafer, de Bono, and Taylor labs (MRC LMB) and Young-Jai You (Nagoya University) for helpful discussions. We sincerely thank Inja Radman for some DNA constructs. Some strains were provided by the CGC, which is funded by the National Institutes of Health (NIH P40 OD010440 ). We are grateful to Dr. Mei Zhen for the RID::Chrimson line ZM9315. This work was funded by grants from the Medical Research Council ( MC-A023-5PB91 ) and the Wellcome Trust ( WT103784MA ) to W.R.S., from the NIH ( R21DC015652 ) to W.R.S. and H.L., from the NIH ( R01NS096581 and R01GM088333 ) to H.L., from the Natural Sciences and Engineering Research Council of Canada (NSERC grant #122216-2013 ) to C.H.R., and from the NIH ( R21DC016258 ) to J.B. Y.L.C. is funded by an EMBO Long-term Fellowship (ALTF 403-2016). A.J.Y. is funded by a NSERC Canada Graduate Scholarship-Master’s (CGS-M). E.L.A. is funded by a NSERC CGS. I.B. is funded by an EMBO Long-term Fellowship (ALTF 387-2015) and is a fellow of the Research Foundation - Flanders (FWO). Publisher Copyright: © 2018 MRC Laboratory of Molecular Biology

PY - 2018/9/19

Y1 - 2018/9/19

N2 - Sensitization is a simple form of behavioral plasticity by which an initial stimulus, often signaling danger, leads to increased responsiveness to subsequent stimuli. Cross-modal sensitization is an important feature of arousal in many organisms, yet its molecular and neural mechanisms are incompletely understood. Here we show that in C. elegans, aversive mechanical stimuli lead to both enhanced locomotor activity and sensitization of aversive chemosensory pathways. Both locomotor arousal and cross-modal sensitization depend on the release of FLP-20 neuropeptides from primary mechanosensory neurons and on their receptor FRPR-3. Surprisingly, the critical site of action of FRPR-3 for both sensory and locomotor arousal is RID, a single neuroendocrine cell specialized for the release of neuropeptides that responds to mechanical stimuli in a FLP-20-dependent manner. Thus, FLP-20 peptides function as an afferent arousal signal that conveys mechanosensory information to central neurons that modulate arousal and other behavioral states. Video Abstract:[Figure presented] Arousal is an important conserved behavioral state where animals show increased sensory responsiveness and locomotor hyperactivity. Chew et al. identify a neuromodulatory pathway that enables mechanosensory neurons to promote both sensory and locomotor arousal via activation of a neuroendocrine center.

AB - Sensitization is a simple form of behavioral plasticity by which an initial stimulus, often signaling danger, leads to increased responsiveness to subsequent stimuli. Cross-modal sensitization is an important feature of arousal in many organisms, yet its molecular and neural mechanisms are incompletely understood. Here we show that in C. elegans, aversive mechanical stimuli lead to both enhanced locomotor activity and sensitization of aversive chemosensory pathways. Both locomotor arousal and cross-modal sensitization depend on the release of FLP-20 neuropeptides from primary mechanosensory neurons and on their receptor FRPR-3. Surprisingly, the critical site of action of FRPR-3 for both sensory and locomotor arousal is RID, a single neuroendocrine cell specialized for the release of neuropeptides that responds to mechanical stimuli in a FLP-20-dependent manner. Thus, FLP-20 peptides function as an afferent arousal signal that conveys mechanosensory information to central neurons that modulate arousal and other behavioral states. Video Abstract:[Figure presented] Arousal is an important conserved behavioral state where animals show increased sensory responsiveness and locomotor hyperactivity. Chew et al. identify a neuromodulatory pathway that enables mechanosensory neurons to promote both sensory and locomotor arousal via activation of a neuroendocrine center.

KW - C. elegans

KW - arousal

KW - behavioral states

KW - neuropeptides

KW - sensitization

UR - http://www.scopus.com/inward/record.url?scp=85054092579&partnerID=8YFLogxK

U2 - 10.1016/j.neuron.2018.08.003

DO - 10.1016/j.neuron.2018.08.003

M3 - Article

C2 - 30146306

AN - SCOPUS:85054092579

SN - 0896-6273

VL - 99

SP - 1233-1246.e6

JO - Neuron

JF - Neuron

IS - 6

ER -

An Afferent Neuropeptide System Transmits Mechanosensory Signals Triggering Sensitization and Arousal in C. elegans

Abstract

Bibliographical note

Keywords

Access to Document

Other files and links

Fingerprint

Cite this