IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0139314.html
   My bibliography  Save this article

TRPM8-Dependent Dynamic Response in a Mathematical Model of Cold Thermoreceptor

Author

Listed:
  • Erick Olivares
  • Simón Salgado
  • Jean Paul Maidana
  • Gaspar Herrera
  • Matías Campos
  • Rodolfo Madrid
  • Patricio Orio

Abstract

Cold-sensitive nerve terminals (CSNTs) encode steady temperatures with regular, rhythmic temperature-dependent firing patterns that range from irregular tonic firing to regular bursting (static response). During abrupt temperature changes, CSNTs show a dynamic response, transiently increasing their firing frequency as temperature decreases and silencing when the temperature increases (dynamic response). To date, mathematical models that simulate the static response are based on two depolarizing/repolarizing pairs of membrane ionic conductance (slow and fast kinetics). However, these models fail to reproduce the dynamic response of CSNTs to rapid changes in temperature and notoriously they lack a specific cold-activated conductance such as the TRPM8 channel. We developed a model that includes TRPM8 as a temperature-dependent conductance with a calcium-dependent desensitization. We show by computer simulations that it appropriately reproduces the dynamic response of CSNTs from mouse cornea, while preserving their static response behavior. In this model, the TRPM8 conductance is essential to display a dynamic response. In agreement with experimental results, TRPM8 is also needed for the ongoing activity in the absence of stimulus (i.e. neutral skin temperature). Free parameters of the model were adjusted by an evolutionary optimization algorithm, allowing us to find different solutions. We present a family of possible parameters that reproduce the behavior of CSNTs under different temperature protocols. The detection of temperature gradients is associated to a homeostatic mechanism supported by the calcium-dependent desensitization.

Suggested Citation

  • Erick Olivares & Simón Salgado & Jean Paul Maidana & Gaspar Herrera & Matías Campos & Rodolfo Madrid & Patricio Orio, 2015. "TRPM8-Dependent Dynamic Response in a Mathematical Model of Cold Thermoreceptor," PLOS ONE, Public Library of Science, vol. 10(10), pages 1-17, October.
    • Handle: RePEc:plo:pone00:0139314
    DOI: 10.1371/journal.pone.0139314
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0139314
    Download Restriction: no
    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0139314&type=printable
    Download Restriction: no
    File URL: https://libkey.io/10.1371/journal.pone.0139314?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. Diana M. Bautista & Jan Siemens & Joshua M. Glazer & Pamela R. Tsuruda & Allan I. Basbaum & Cheryl L. Stucky & Sven-Eric Jordt & David Julius, 2007. "The menthol receptor TRPM8 is the principal detector of environmental cold," Nature, Nature, vol. 448(7150), pages 204-208, July.
    2. X.-M. Xia & B. Fakler & A. Rivard & G. Wayman & T. Johnson-Pais & J. E. Keen & T. Ishii & B. Hirschberg & C. T. Bond & S. Lutsenko & J. Maylie & J. P. Adelman, 1998. "Mechanism of calcium gating in small-conductance calcium-activated potassium channels," Nature, Nature, vol. 395(6701), pages 503-507, October.
    3. Thomas Voets & Guy Droogmans & Ulrich Wissenbach & Annelies Janssens & Veit Flockerzi & Bernd Nilius, 2004. "The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels," Nature, Nature, vol. 430(7001), pages 748-754, August.
    4. David D. McKemy & Werner M. Neuhausser & David Julius, 2002. "Identification of a cold receptor reveals a general role for TRP channels in thermosensation," Nature, Nature, vol. 416(6876), pages 52-58, March.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Budzinski, R.C. & Boaretto, B.R.R. & Prado, T.L. & Lopes, S.R., 2019. "Temperature dependence of phase and spike synchronization of neural networks," Chaos, Solitons & Fractals, Elsevier, vol. 123(C), pages 35-42.

    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. Cheng Zhao & Yuan Xie & Lizhen Xu & Fan Ye & Ximing Xu & Wei Yang & Fan Yang & Jiangtao Guo, 2022. "Structures of a mammalian TRPM8 in closed state," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Ivo B. Regli & Giacomo Strapazzon & Marika Falla & Rosmarie Oberhammer & Hermann Brugger, 2021. "Long-Term Sequelae of Frostbite—A Scoping Review," IJERPH, MDPI, vol. 18(18), pages 1-16, September.
    3. David Alarcón-Alarcón & David Cabañero & Jorge Andrés-López & Magdalena Nikolaeva-Koleva & Simona Giorgi & Gregorio Fernández-Ballester & Asia Fernández-Carvajal & Antonio Ferrer-Montiel, 2022. "TRPM8 contributes to sex dimorphism by promoting recovery of normal sensitivity in a mouse model of chronic migraine," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    4. Hiroki Ota & Kimiaki Katanosaka & Shiori Murase & Makiko Kashio & Makoto Tominaga & Kazue Mizumura, 2013. "TRPV1 and TRPV4 Play Pivotal Roles in Delayed Onset Muscle Soreness," PLOS ONE, Public Library of Science, vol. 8(6), pages 1-10, June.
    5. 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.
    6. Michael A Ha & Gregory J Smith & Joseph A Cichocki & Lu Fan & Yi-Shiuan Liu & Ana I Caceres & Sven Eric Jordt & John B Morris, 2015. "Menthol Attenuates Respiratory Irritation and Elevates Blood Cotinine in Cigarette Smoke Exposed Mice," PLOS ONE, Public Library of Science, vol. 10(2), pages 1-16, February.
    7. WHO Study Group on Tobacco Product Regulation (TobReg), 2016. "Advisory note: banning menthol in tobacco products," University of California at San Francisco, Center for Tobacco Control Research and Education qt8td7w55n, Center for Tobacco Control Research and Education, UC San Francisco.
    8. Lavanya Moparthi & Viktor Sinica & Vamsi K. Moparthi & Mohamed Kreir & Thibaut Vignane & Milos R. Filipovic & Viktorie Vlachova & Peter M. Zygmunt, 2022. "The human TRPA1 intrinsic cold and heat sensitivity involves separate channel structures beyond the N-ARD domain," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Jing Lei & Reiko U. Yoshimoto & Takeshi Matsui & Masayuki Amagai & Mizuho A. Kido & Makoto Tominaga, 2023. "Involvement of skin TRPV3 in temperature detection regulated by TMEM79 in mice," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    10. Chang-Hyung Lee & Young-A Choi & Sung-Jin Heo & Parkyong Song, 2021. "The Effect of Hyperbaric Therapy on Brown Adipose Tissue in Rats," IJERPH, MDPI, vol. 18(17), pages 1-8, August.
    11. Patricia Aroni & Ligia F. Fonseca & Marcia A. Ciol & Amanda S. Margatho & Cristina M. Galvão, 2020. "The use of mentholated popsicle to reduce thirst during preoperative fasting: A randomised controlled trial," Journal of Clinical Nursing, John Wiley & Sons, vol. 29(5-6), pages 840-851, March.

    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:pone00:0139314. 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.