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ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2021; 67(1): 44-56


STRUCTURE, PROPERTIES AND PHYSIOLOGICAL ROLE OF TRPA1 RECEPTORS

M.A. Petrushenko, E.A. Petrushenko, E.A. Lukyanetz

  1. Bogomoletz Institute of physiology NAS of Ukraine, Kyiv, Ukraine, Ukraine
DOI: https://doi.org/10.15407/fz67.01.044


Abstract

In mammals, the ankyrin ionotropic transient receptor potential type 1 (TRPA1) is the only member of the TRPA receptor gene subfamily. It is defined as a target for damaging and inflammatory effects in peripheral sensory neurons, which implies its functional role in the development of pain and neurogenic inflammation. Experimental studies indicate that calcium permeable non-selective ion receptor channel TRPA1 is activated by a number of exogenous irritant compounds, factors including low temperatures. This review describes the structure, properties, and physiological role of TRPA1 receptors.

Keywords: TRPA1 channels; TRPA1 receptors; calcium channels; neuropathy; diabetic neuropathy; neurons; pain sensitivity

References

  1. Clapham DE. Pain-sensing TRPA1 channel resolved. Nature. 2015;520(7548):439-41. CrossRef PubMed
  2. Jaquemar D, Schenker T, Trueb B. An ankyrin-like protein with transmembrane domains is specifically lost after oncogenic transformation of human fibroblasts. J Biol Chem. 1999;274(11):7325-33. CrossRef PubMed
  3. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell. 2003;112(6):819-29. CrossRef
  4. Jiang Y, Lee A, Chen J, Ruta V, Cadene M, Chait BT, et al. X-ray structure of a voltage-dependent K+ channel. Nature. 2003;423(6935):33-41. CrossRef PubMed
  5. Zayats V, Samad A, Minofar B, Roelofs KE, Stockner T, Ettrich R. Regulation of the transient receptor potential channel TRPA1 by its N-terminal ankyrin repeat domain. J Mol Model. 2013;19(11):4689-700. CrossRef PubMed
  6. Ladrón-de-Guevara E, Rangel-Yescas GE, FernándezVelasco DA, Torres-Larios A, Rosenbaum T, Islas LD. The contribution of the ankyrin repeat domain of TRPV1 as a thermal module. BioRxiv. 2019:641803. CrossRef PubMedCentral
  7. Brewster MSJ, Gaudet R. How the TRPA1 receptor transmits painful stimuli: Inner workings revealed by electron cryomicroscopy. Bioessays. 2015;37(11): 1184-92. CrossRef PubMed PubMedCentral
  8. Souza Monteiro de Araujo D, Nassini R, Geppetti P, De Logu F. TRPA1 as a therapeutic target for nociceptive pain. Exp Opin Ther Targets. 2020;24(10):997-1008. CrossRef PubMed
  9. Koivisto A, Jalava N, Bratty R, Pertovaara A. TRPA1 Antagonists for Pain Relief. 2018;11(4). CrossRef PubMed PubMedCentral
  10. Zurborg S. Defining a function for the ion channel TRPA1 [DISSERTATION ]. Berlin: Charité - Universitätsmedizin 2009.
  11. Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, Poblete J, et al. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell. 2006;124(6):1269-82. CrossRef PubMed
  12. Simons CT, Carstens MI, Carstens E. Oral irritation by mustard oil: self-desensitization and cross-desensitization with capsaicin. Chem Senses. 2003;28(6):459-65. CrossRef PubMed
  13. Anand U, Otto WR, Facer P, Zebda N, Selmer I, Gunthorpe MJ, et al. TRPA1 receptor localisation in the human peripheral nervous system and functional studies in cultured human and rat sensory neurons. Neurosci Lett. 2008;438(2):221-7. CrossRef PubMed
  14. Dragan AV, Petrushenko OA, Burlak OP, Lukyanetz EA. Effect of TRPA1 receptor activation on TRPV1 channel desensitization in rat dorsal ganglion neurons. Fiziol Zh. 2016;62(1):16-24. CrossRef PubMed
  15. Guimaraes MZP, Jordt SE. Frontiers in Neuroscience. TRPA1: A Sensory Channel of Many Talents. In: Liedtke WB, Heller S, editors. TRP Ion Channel Function in Sensory Transduction and Cellular Signaling Cascades. Boca Raton (FL): CRC Press/Taylor & Francis Taylor & Francis Group, LLC.; 2007.
  16. Hinman A, Chuang HH, Bautista DM, Julius D. TRP channel activation by reversible covalent modification. Proc Natl Acad Sci USA. 2006;103(51):19564-8. CrossRef PubMed PubMedCentral
  17. Akopian AN, Ruparel NB, Jeske NA, Hargreaves KM. Transient receptor potential TRPA1 channel desensitization in sensory neurons is agonist dependent and regulated by TRPV1-directed internalization. J Physiol. 2007;583(Part 1):175-93. CrossRef PubMed PubMedCentral
  18. Kim D, Cavanaugh EJ. Requirement of a soluble intracellular factor for activation of transient receptor potential A1 by pungent chemicals: role of inorganic polyphosphates. J Neurosci. 2007;27(24):6500-9. CrossRef PubMed PubMedCentral
  19. Choi S-I, Hwang SW. depolarizing effectors of bradykinin signaling in nociceptor excitation in pain perception. Biomol Ther (Seoul). 2018;26(3):255-67. CrossRef PubMed PubMedCentral
  20. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, et al. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron. 2004;41(6):849-57. CrossRef
  21. Sawada Y, Hosokawa H, Hori A, Matsumura K, Kobayashi S. Cold sensitivity of recombinant TRPA1 channels. Brain Res. 2007;1160:39-46. CrossRef PubMed
  22. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Hogestatt ED, et al. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature. 2004;427(6971):260-5. CrossRef PubMed
  23. Chen J, Joshi SK, DiDomenico S, Perner RJ, Mikusa JP, Gauvin DM, et al. Selective blockade of TRPA1 channel attenuates pathological pain without altering noxious cold sensation or body temperature regulation. Pain. 2011;152(5):1165-72. CrossRef PubMed
  24. Chen J, Hackos DH. TRPA1 as a drug target-promise and challenges. Naunyn-Schmiedeberg's Arch Pharmac. 2015;388(4):451-63. CrossRef PubMed PubMedCentral
  25. Laursen WJ, Anderson EO, Hoffstaetter LJ, Bagriantsev SN, Gracheva EO. Species-specific temperature sensitivity of TRPA1. Temperature. 2015;2(2):214-26. CrossRef PubMed PubMedCentral
  26. Moparthi L, Kichko TI, Eberhardt M, Högestätt ED, Kjellbom P, Johanson U, et al. Human TRPA1 is a heat sensor displaying intrinsic U-shaped thermosensitivity. Sci Rep. 2016;6(1):28763. CrossRef PubMed PubMedCentral
  27. Hasan R, Leeson-Payne ATS, Jaggar JH, Zhang X. Calmodulin is responsible for Ca2+-dependent regulation of TRPA1 Channels. Sci Rep. 2017;7(1):45098. CrossRef PubMed PubMedCentral
  28. Wang YY, Chang RB, Waters HN, McKemy DD, Liman ER. The nociceptor ion channel TRPA1 is potentiated and inactivated by permeating calcium ions. J Biol Chem. 2008;283(47):32691-703. CrossRef PubMed PubMedCentral
  29. Lukyanetz EA, Sotkis AV, Kostyuk PG. Mechanisms of up-regulation of single calcium channels by serotonin in Helix pomatia neurons. Biochem Biophys Res Commun. 2002;293(1):132-8. CrossRef
  30. Lukyanetz EA, Sotkis AV. Serotonin-induced changes in the activity of single Ca2+ channels in Helix pomatia neurons. Neurophysiology; 1996: Kluwer Academic Publishers-Plenum Publishers; 1996. p. 103-10. CrossRef
  31. Zurborg S, Yurgionas B, Jira JA, Caspani O, Heppenstall PA. Direct activation of the ion channel TRPA1 by Ca2+. Nat Neurosci. 2007;10(3):277-9. CrossRef PubMed
  32. Doerner JF, Gisselmann G, Hatt H, Wetzel CH. Transient receptor potential channel A1 is directly gated by calcium ions. J Biol Chem. 2007;282(18):13180-9. CrossRef PubMed
  33. Doroshenko PA, Kostyuk PG, Luk'yanetz EA. Modulation of calcium current by calmodulin antagonists. Neuroscience. 1988;27(3):1073-80. CrossRef
  34. Peterson BZ, DeMaria CD, Adelman JP, Yue DT. Calmodulin is the Ca2+ sensor for Ca2+-dependent inactivation of L-type calcium channels. Neuron. 1999;22(3):549-58. CrossRef
  35. Lee A, Wong ST, Gallagher D, Li B, Storm DR, Scheuer T, et al. Ca2+/calmodulin binds to and modulates P/Qtype calcium channels. Nature. 1999;399(6732):155-9. CrossRef PubMed
  36. Zuhlke RD, Pitt GS, Deisseroth K, Tsien RW, Reuter H. Calmodulin supports both inactivation and facilitation of L-type calcium channels. Nature. 1999;399(6732):159-62. CrossRef PubMed
  37. Moparthi L, Moparthi SB, Wenger J, Zygmunt PM. Calcium activates purified human TRPA1 with and without its N-terminal ankyrin repeat domain in the absence of calmodulin. bioRxiv. 2020:2020.03.19.999276. CrossRef PubMedCentral
  38. Kostyuk PG, Lukyanetz EA, Doroshenko PA. Effects of serotonin and cAMP on calcium currents in different neurones of Helix pomatia. Pflüg Arch Eur J Physiol. 1992;420(1):9-15. CrossRef PubMed
  39. Lukyanetz EA, Kostyuk PG. Two distinct receptors operate the cAMP cascade to up-regulate L-type Ca channels. Pflüg Arch. 1996;432(2):174-81. CrossRef PubMed
  40. Kostyuk PG, Lukyanetz EA, Ter-Markosyan AS. Parathyroid hormone enhances calcium current in snail neurones - Simulation of the effect by phorbol esters. Pflüg Arch. 1992;420(2):146-52. CrossRef PubMed
  41. Kostyuk PG, Lukyanetz EA. Mechanisms of antagonistic action of internal Ca2+ on serotonin-induced potentiation of Ca2+ currents in Helix neurones. Pflüg Arch. 1993;424(1):73-83. CrossRef PubMed
  42. Lukyanetz EA. Role of calcineurin in regulation of high voltage-activated calcium channel activity. Neurophysiology. 1997;29(6):352-6. CrossRef
  43. Lukyanetz EA. Evidence for colocalization of calcineurin and calcium channels in dorsal root ganglion neurons. Neuroscience. 1997;78(3):625-8. CrossRef
  44. Liu D, Liman ER. Intracellular Ca2+ and the phospholipid PIP2 regulate the taste transduction ion channel TRPM5. Proc Natl Acad Sci USA. 2003;100(25):15160-5. CrossRef PubMed PubMedCentral
  45. Liu B, Zhang C, Qin F. Functional recovery from desensitization of vanilloid receptor TRPV1 requires resynthesis of phosphatidylinositol 4,5-bisphosphate. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2005;25(19):4835-43. CrossRef PubMed PubMedCentral
  46. Zhang Z, Okawa H, Wang Y, Liman ER. Phosphatidylinositol 4,5-bisphosphate rescues TRPM4 channels from desensitization. J Biol Chem. 2005;280(47):39185-92. CrossRef PubMed
  47. Weng HJ, Patel KN, Jeske NA, Bierbower SM, Zou W, Tiwari V, et al. Tmem100 is a regulator of TRPA1-TRPV1 complex and contributes to persistent pain. Neuron. 2015;85(4):833-46. CrossRef PubMed PubMedCentral
  48. Dubin AE, Patapoutian A. Nociceptors: the sensors of the pain pathway. J Clin Invest. 2010;120(11):3760-72. CrossRef PubMed PubMedCentral
  49. McNamara CR, Mandel-Brehm J, Bautista DM, Siemens J, Deranian KL, Zhao M, et al. TRPA1 mediates formalin-induced pain. Proc Natl Acad Sci USA. 2007;104(33):13525-30. CrossRef PubMed PubMedCentral
  50. Meseguer V, Alpizar YA, Luis E, Tajada S, Denlinger B, Fajardo O, et al. TRPA1 channels mediate acute neurogenic inflammation and pain produced by bacterial endotoxins. Nat Commun. 2014;5:3125. CrossRef PubMed PubMedCentral
  51. Petrushenko OA, Lukyanetz EA. Some physiological mechanisms functioning in models of pain-related processes. Neurophysiology. 2019;51(3):223-31. CrossRef
  52. Andersson DA, Gentry C, Light E, Vastani N, Vallortigara J, Bierhaus A, et al. Methylglyoxal evokes pain by stimulating TRPA1. PloS One. 2013;8(10):e77986. CrossRef PubMed PubMedCentral
  53. Cao DS, Zhong L, Hsieh TH, Abooj M, Bishnoi M, Hughes L, et al. Expression of transient receptor potential ankyrin 1 (TRPA1) and its role in insulin release from rat pancreatic beta cells. PloS One. 2012;7(5):e38005. CrossRef PubMed PubMedCentral
  54. Numazawa S, Takase M, Ahiko T, Ishii M, Shimizu S, Yoshida T. Possible involvement of transient receptor potential channels in electrophile-induced insulin secretion from RINm5F cells. Biol Pharm Bull. 2012;35(3):346-54. CrossRef PubMed
  55. Anand P, Murali KY, Tandon V, Murthy PS, Chandra R. Insulinotropic effect of cinnamaldehyde on transcriptional regulation of pyruvate kinase, phosphoenolpyruvate carboxykinase, and GLUT4 translocation in experimental diabetic rats. Chem Biol Interact. 2010;186(1):72-81. CrossRef PubMed
  56. Babes A, Fischer MJ, Filipovic M, Engel MA, Flonta ML, Reeh PW. The anti-diabetic drug glibenclamide is an agonist of the transient receptor potential Ankyrin 1 (TRPA1) ion channel. Eur J Pharmacol. 2013;704(1-3):15-22. CrossRef PubMed
  57. Derbenev AV, Zsombok A. Potential therapeutic value of TRPV1 and TRPA1 in diabetes mellitus and obesity. Semin Immunopathol. 2016;38(3):397-406. CrossRef PubMed PubMedCentral
  58. Mang B, Wolters M, Schmitt B, Kelb K, Lichtinghagen R, Stichtenoth DO, et al. Effects of a cinnamon extract on plasma glucose, HbA, and serum lipids in diabetes mellitus type 2. Eur J Clin Invest. 2006;36(5):340-4. CrossRef PubMed
  59. Khan A, Safdar M, Ali Khan MM, Khattak KN, Anderson RA. Cinnamon improves glucose and lipids of people with type 2 diabetes. Diabetes Care. 2003;26(12):3215-8. CrossRef PubMed
  60. Ahn J, Lee H, Im SW, Jung CH, Ha TY. Allyl isothiocyanate ameliorates insulin resistance through the regulation of mitochondrial function. J Nutr Biochem. 2014;25(10):1026-34. CrossRef PubMed
  61. Koivisto A, Pertovaara A. Transient receptor potential ankyrin 1 (TRPA1) ion channel in the pathophysiology of peripheral diabetic neuropathy. Scand J Pain. 2013;4(3):129-36. CrossRef PubMed

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