IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0196954.html
   My bibliography  Save this article

Monoamines differentially modulate neuropeptide release from distinct sites within a single neuron pair

Author

Listed:
  • Tobias Clark
  • Vera Hapiak
  • Mitchell Oakes
  • Holly Mills
  • Richard Komuniecki

Abstract

Monoamines and neuropeptides often modulate the same behavior, but monoaminergic-peptidergic crosstalk remains poorly understood. In Caenorhabditis elegans, the adrenergic-like ligands, tyramine (TA) and octopamine (OA) require distinct subsets of neuropeptides in the two ASI sensory neurons to inhibit nociception. TA selectively increases the release of ASI neuropeptides encoded by nlp-14 or nlp-18 from either synaptic/perisynaptic regions of ASI axons or the ASI soma, respectively, and OA selectively increases the release of ASI neuropeptides encoded by nlp-9 asymmetrically, from only the synaptic/perisynaptic region of the right ASI axon. The predicted amino acid preprosequences of genes encoding either TA- or OA-dependent neuropeptides differed markedly. However, these distinct preprosequences were not sufficient to confer monoamine-specificity and additional N-terminal peptide-encoding sequence was required. Collectively, our results demonstrate that TA and OA specifically and differentially modulate the release of distinct subsets of neuropeptides from different subcellular sites within the ASIs, highlighting the complexity of monoaminergic/peptidergic modulation, even in animals with a relatively simple nervous system.

Suggested Citation

  • Tobias Clark & Vera Hapiak & Mitchell Oakes & Holly Mills & Richard Komuniecki, 2018. "Monoamines differentially modulate neuropeptide release from distinct sites within a single neuron pair," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-22, May.
  • Handle: RePEc:plo:pone00:0196954
    DOI: 10.1371/journal.pone.0196954
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0196954
    Download Restriction: no

    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0196954&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pone.0196954?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Min Guo & Tai-Hong Wu & Yan-Xue Song & Ming-Hai Ge & Chun-Ming Su & Wei-Pin Niu & Lan-Lan Li & Zi-Jing Xu & Chang-Li Ge & Maha T. H. Al-Mhanawi & Shi-Ping Wu & Zheng-Xing Wu, 2015. "Reciprocal inhibition between sensory ASH and ASI neurons modulates nociception and avoidance in Caenorhabditis elegans," Nature Communications, Nature, vol. 6(1), pages 1-13, May.
    2. Thomas Euler & Peter B. Detwiler & Winfried Denk, 2002. "Directionally selective calcium signals in dendrites of starburst amacrine cells," Nature, Nature, vol. 418(6900), pages 845-852, August.
    3. Sreekanth H. Chalasani & Nikos Chronis & Makoto Tsunozaki & Jesse M. Gray & Daniel Ramot & Miriam B. Goodman & Cornelia I. Bargmann, 2007. "Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans," Nature, Nature, vol. 450(7166), pages 63-70, November.
    4. Lavinia Palamiuc & Tallie Noble & Emily Witham & Harkaranveer Ratanpal & Megan Vaughan & Supriya Srinivasan, 2017. "A tachykinin-like neuroendocrine signalling axis couples central serotonin action and nutrient sensing with peripheral lipid metabolism," Nature Communications, Nature, vol. 8(1), pages 1-14, April.
    5. Hiroshi Suzuki & Tod R. Thiele & Serge Faumont & Marina Ezcurra & Shawn R. Lockery & William R. Schafer, 2008. "Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis," Nature, Nature, vol. 454(7200), pages 114-117, July.
    6. Paul D. Wes & Cornelia I. Bargmann, 2001. "C. elegans odour discrimination requires asymmetric diversity in olfactory neurons," Nature, Nature, vol. 410(6829), pages 698-701, April.
    7. Michael Hendricks & Heonick Ha & Nicolas Maffey & Yun Zhang, 2012. "Compartmentalized calcium dynamics in a C. elegans interneuron encode head movement," Nature, Nature, vol. 487(7405), pages 99-103, July.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Chenxi Lin & Yuxin Shan & Zhongyi Wang & Hui Peng & Rong Li & Pingzhou Wang & Junyan He & Weiwei Shen & Zhengxing Wu & Min Guo, 2024. "Molecular and circuit mechanisms underlying avoidance of rapid cooling stimuli in C. elegans," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Javier J How & Saket Navlakha & Sreekanth H Chalasani, 2021. "Neural network features distinguish chemosensory stimuli in Caenorhabditis elegans," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-38, November.
    3. Jen-Chun Hsiang & Ning Shen & Florentina Soto & Daniel Kerschensteiner, 2024. "Distributed feature representations of natural stimuli across parallel retinal pathways," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    4. Hillary A. Miller & Shijiao Huang & Elizabeth S. Dean & Megan L. Schaller & Angela M. Tuckowski & Allyson S. Munneke & Safa Beydoun & Scott D. Pletcher & Scott F. Leiser, 2022. "Serotonin and dopamine modulate aging in response to food odor and availability," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    5. Yuxiao Hua & Yuki Todo & Zheng Tang & Sichen Tao & Bin Li & Riku Inoue, 2022. "A Novel Bio-Inspired Motion Direction Detection Mechanism in Binary and Grayscale Background," Mathematics, MDPI, vol. 10(20), pages 1-16, October.
    6. Andrew Jo & Sercan Deniz & Jian Xu & Robert M. Duvoisin & Steven H. DeVries & Yongling Zhu, 2023. "A sign-inverted receptive field of inhibitory interneurons provides a pathway for ON-OFF interactions in the retina," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    7. Yeon Jin Kim & Beth B. Peterson & Joanna D. Crook & Hannah R. Joo & Jiajia Wu & Christian Puller & Farrel R. Robinson & Paul D. Gamlin & King-Wai Yau & Felix Viana & John B. Troy & Robert G. Smith & O, 2022. "Origins of direction selectivity in the primate retina," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    8. Andrew Jo & Sercan Deniz & Suraj Cherian & Jian Xu & Daiki Futagi & Steven H. DeVries & Yongling Zhu, 2023. "Modular interneuron circuits control motion sensitivity in the mouse retina," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. Zhongyu Chen & Yuguo Yu & Xiangyang Xue, 2023. "A Connectome-Based Digital Twin Caenorhabditis elegans Capable of Intelligent Sensorimotor Behavior," Mathematics, MDPI, vol. 11(11), pages 1-23, May.
    10. Xiliang Zhang & Sichen Tao & Zheng Tang & Shuxin Zheng & Yoki Todo, 2023. "The Mechanism of Orientation Detection Based on Artificial Visual System for Greyscale Images," Mathematics, MDPI, vol. 11(12), pages 1-13, June.
    11. Héctor Acarón Ledesma & Jennifer Ding & Swen Oosterboer & Xiaolin Huang & Qiang Chen & Sui Wang & Michael Z. Lin & Wei Wei, 2024. "Dendritic mGluR2 and perisomatic Kv3 signaling regulate dendritic computation of mouse starburst amacrine cells," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    12. Sichen Tao & Yuki Todo & Zheng Tang & Bin Li & Zhiming Zhang & Riku Inoue, 2022. "A Novel Artificial Visual System for Motion Direction Detection in Grayscale Images," Mathematics, MDPI, vol. 10(16), pages 1-32, August.
    13. Chung-Chih Liu & Ayub Khan & Nicolas Seban & Nicole Littlejohn & Aayushi Shah & Supriya Srinivasan, 2024. "A homeostatic gut-to-brain insulin antagonist restrains neuronally stimulated fat loss," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pone00:0196954. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.