Українська English

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. 2023; 69(1): 68-76

ACID-SENSING ION CHANNELS: THE ROLE IN HIGHER ORDER BRAIN FUNCTIONS

V.I. Kravchenko1, A.V. Venhreniuk2, A.O. Cherninskyi2

  1. Taras Shevchenko National University of Kyiv, Ukraine
  2. Bogomoletz Institute of Physiology, National Academy of Sciences of Ukraine, Kyiv, Ukraine
DOI: https://doi.org/10.15407/fz69.01.068


Abstract

Acid-sensing ion channels (ASICs) are ionotropic receptors that generate an inward cationic current in response to a relatively rapid drop in extracellular pH. They were found in the membranes of neurons and glial cells. In the peripheral nervous system, ASICs are involved, in particular, in nociception. More intriguing is the role of these channels in the functioning of the central nervous system. They are widely expressed in brain regions involved in systemic, integrative functions. This review is devoted to the role of ASICs in the implementation of higher-order information processing like emotional regulation, fear extinction, spatial memory, and different forms of learning.

Keywords: acid-sensing ion channels; anxiolytic action; spatial memory; associative learning; fear; addiction.

Full text: (PDF, in Ukrainian)

References

  1. Krishtal O, Pidoplichko V. A receptor for protons in the nerve cell membrane. Neuroscience. 1980;5:2325-7. CrossRef PubMed
  2. Hill A, Ben-Shahar Y. The synaptic action of degenerin/ epithelial sodium channels. Channels (Austin). 2018; 12(1):262-75. CrossRef PubMed PubMedCentral
  3. Zha X. Acid-sensing ion channels: trafficking and synaptic function. Mol Brain. 2013 Jan 2;6:1. CrossRef PubMed PubMedCentral
  4. Carattino M, Montalbetti N. Acid-sensing ion channels in sensory signaling. Am J Physiol Renal Physiol. 2020 Mar 1;318(3):F531-43. CrossRef PubMed PubMedCentral
  5. Storozhuk M, Cherninskyi A, Maximyuk O, Isaev D, Krishtal O. Acid-sensing ion channels: Focus on physiological and some pathological roles in the brain. Curr Neuropharmacol. 2021;19(9):1570-89. CrossRef PubMed PubMedCentral
  6. Wemmie J, Askwith C, Lamani E, Cassell M, Freeman J, Welsh M. Acid-sensing ion channel 1 is localized in brain regions with high synaptic density and contributes to fear conditioning. J Neurosci. 2003 Jul 2;23(13):5496-502. CrossRef PubMed PubMedCentral
  7. Wemmie J, Coryell M, Askwith C, Lamani E, Leonard A, Sigmund C, Welsh M. Overexpression of acid-sensing ion channel 1a in transgenic mice increases acquired fear-related behavior. Proc Natl Acad Sci USA. 2004 Mar 9;101(10):3621-6. CrossRef PubMed PubMedCentral
  8. Coryell M, Wunsch A, Haenfler J, Allen J, Schnizler M, Ziemann A, et al. Acid-sensing ion channel-1a in the amygdala, a novel therapeutic target in depression-related behavior. J Neurosci. 2009 Apr 29;29(17):5381-8. CrossRef PubMed PubMedCentral
  9. Kreple C, Lu Y, Taugher R, Schwager-Gutman A, Du J, Stump M, et al. Acid-sensing ion channels contribute to synaptic transmission and inhibit cocaine-evoked plasticity. Nat Neurosci. 2014 Aug;17(8):1083-91. CrossRef PubMed PubMedCentral
  10. Coryell M, Ziemann A, Westmoreland P, Haenfler J, Kurjakovic Z, Zha X, et al. Targeting ASIC1a reduces innate fear and alters neuronal activity in the fear circuit. Biol Psychiatr. 2007 Nov 15;62(10):1140-8. CrossRef PubMed
  11. Pidoplichko V, Aroniadou-Anderjaska V, Prager E, Figueiredo T, Almeida-Suhett C, Miller S, Braga M. ASIC1a activation enhances inhibition in the basolateral amygdala and reduces anxiety. J Neurosci. 2014 Feb 26;34(9):3130-41. CrossRef PubMed PubMedCentral
  12. Baron A, Lingueglia E. Pharmacology of acid-sensing ion channels - physiological and therapeutical perspectives. Neuropharmacology. 2015;94:19-35. CrossRef PubMed
  13. Buta A, Maximyuk O, Kovalskyy D, Sukach V, Vovk M, Ievglevskyi O, et al. Novel potent orthosteric antagonist of ASIC1a prevents NMDAR-dependent LTP induction. J Med Chem 2015,58:4449-61. CrossRef PubMed
  14. Qi X, Jian-Fei L, Zi-Yue H, Yi-Jun L, Lu-Bing C, XinLan W, et al. Pharmacological validation of ASIC1a as a druggable target for neuroprotection in cerebral ischemia using an intravenously available small molecule inhibitor. Front Pharmacol. 2022 Mar 24;13:849498. CrossRef PubMed PubMedCentral
  15. Fedoriuk М, Stefanenko М, Bohovyk R, Cherninskyi A, Maximyuk O, Isaev D, Platonov M, Krishtal O. Pharmacological blockade of acid sensing ion channels normalizes emotionally conditioned learning disturbed due to epileptic status. Fiziol Zh. 2020;66(5):11-6. CrossRef
  16. La-Vu M, Tobias B, Schuette P, Adhikari A. To approach or avoid: An introductory overview of the study of anxiety using rodent assays. Front Behav Neurosci. 2020 Aug 26;14:145. CrossRef PubMed PubMedCentral
  17. Harro J. Animals, anxiety, and anxiety disorders: How to measure anxiety in rodents and why. Behav Brain Res. 2018 Oct 15;352:81-93. CrossRef PubMed
  18. Harmata G, Chan A, Merfeld M, Taugher-Hebl R, Harijan A, Hardie J, et al. Intoxicating effects of alcohol depend on acid-sensing ion channels. Neuropsychopharmacology. 2022 Oct 15. CrossRef PubMed
    19. Dwyer J, Rizzo S, Neal S, Lin Q, Jow F, Arias R, et al. Acid sensing ion channel (ASIC) inhibitors exhibit anxiolyticlike activity in preclinical pharmacological models. Psychopharmacology (Berl). 2009 Mar;203(1):41-52 CrossRef PubMed
  19. Price M, Gong H, Parsons M, Kundert J, Reznikov L, Bernardinelli L, et al. Localization and behaviors in null mice suggest that ASIC1 and ASIC2 modulate responses to aversive stimuli. Genes Brain Behav. 2014 Feb;13(2):179-94. CrossRef PubMed PubMedCentral
  20. Ievglevskyi O, Isaev D, Netsyk O, Romanov A, Fedoriuk M, Maximyuk O, et al. Acid-sensing ion channels regulate spontaneous inhibitory activity in the hippocampus: possible implications for epilepsy. Philos Trans Roy Soc Lond B Biol Sci. 2016 Aug 5;371(1700):20150431. CrossRef PubMed PubMedCentral
  21. Fedoriuk MP, Cherninskyi AO, Maximyuk OP, Isaev DS, Bogovyk RI, Venhreniuk AV, Boyko OM, Krishtal OO. Inhibition of brain ASICs affects hippocampal thetarhythm and openfield behavior in rats. Fiziol Zh. 2019; 65(1):15-19. CrossRef
  22. Yellepeddi V, Sayre C, Burrows A, Watt K, Davies S, Strauss J, Battaglia M. Stability of extemporaneously compounded amiloride nasal spray. PLoS One. 2020 Jul 10;15(7):e0232435. CrossRef PubMed PubMedCentral
  23. Azzeh M, Battaglia M, Davies S, Strauss J, Dogra P, Yellepeddi V. Novel intranasal treatment for anxiety disorders using amiloride, an acid-sensing ion channel antagonist: Pharmacokinetic modeling and simulation. Int J Clin Pharmacol Ther. 2022 Jun;60(6):253-63. CrossRef PubMed
  24. Jiang Q, Li M, Papasian C, Branigan D, Xiong Z, Wang J, Chu X. Characterization of acid-sensing ion channels in medium spiny neurons of mouse striatum. Neuroscience. 2009 Aug 4;162(1):55-66. 26. Wemmie J, Chen J, Askwith C, Hruska-Hageman A, Price M, Nolan B, et al. The acid-activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron. 2002 Apr 25;34(3):463-77. CrossRef PubMed
  25. Yu Z, Wu Y, Wang Y, Liu D, Song X, Jiang Q, et al. The acid-sensing ion channel ASIC1a mediates striatal synapse remodeling and procedural motor learning. Sci Sign. 2018 Aug 7;11(542):eaar4481. CrossRef PubMed PubMedCentral
  26. Wu P, Huang Y, Chen C, Hsu T, Lin Y, Weng J, Chien T, Cheng I, Lien C. Acid-sensing ion channel-1a is not required for normal hippocampal LTP and spatial memory. J Neurosci. 2013 Jan 30;33(5):1828-32. CrossRef PubMed PubMedCentral
  27. Wang L, Yi Y, Yao Y, Feng G, Shu C, Wang H, Zhang X. Walnut oil improves spatial memory in rats and increases the expression of acid-sensing ion channel genes Asic2a and Asic4. Food Sci Nutr. 2018 Nov 28;7(1):293-301. CrossRef PubMed PubMedCentral
  28. Rosen J, Asok A, Chakraborty T. The smell of fear: innate threat of 2,5-dihydro-2,4,5-trimethylthiazoline, a single molecule component of a predator odor. Front Neurosci. 2015 Aug 25;9:292. CrossRef
  29. Taugher R, Lu Y, Fan R, Ghobbeh A, Kreple C, Faraci F, Wemmie J. ASIC1A in neurons is critical for fear-related behaviors. Genes Brain Behav. 2017 Nov;16(8):745-55. CrossRef PubMed PubMedCentral
  30. Coryell M, Wunsch A, Haenfler J, Allen J, McBride J, Davidson B, Wemmie J. Restoring acid-sensing ion channel-1a in the amygdala of knock-out mice rescues fear memory but not unconditioned fear responses. J Neurosci. 2008 Dec 17;28(51):13738-41. CrossRef PubMed PubMedCentral
  31. Chiang P, Chien T, Chen C, Yanagawa Y, Lien C. ASICdependent LTP at multiple glutamatergic synapses in amygdala network is required for fear memory. Sci Rep. 2015 May 19;5:10143. CrossRef PubMed PubMedCentral
  32. Wang, Q, Wang Q, Song X, Jiang Q, Wu Y, Li Y, Yuan T, Zhang S, Xu N, Zhu MX, Li W, Xu T. Fear extinction requires ASIC1a-dependent regulation of hippocampalprefrontal correlates. Sci Advanc. 2018;4. CrossRef PubMed PubMedCentral
  33. Li W, Liu M, Deng S, Liu Y, Shang L, Ding J, Hsu T, Jiang Q, Li F, Zhu M, Xu T. ASIC1a regulates insular long-term depression and is required for the extinction of conditioned taste aversion. Nat Commun. 2016 Dec 7;7:13770. CrossRef PubMed PubMedCentral
  34. Kayyal H, Yiannakas A, Kolatt Chandran S, Khamaisy M, Sharma V, Rosenblum K. Activity of insula to basolateral amygdala projecting neurons is necessary and sufficient for taste valence representation. J Neurosci. 2019 Nov 20;39(47):9369-82. CrossRef PubMed PubMedCentral
  35. Feinstein J, Buzza C, Hurlemann R, Follmer R, Dahdaleh N, Coryell W, Welsh M, Tranel D, Wemmie J. Fear and panic in humans with bilateral amygdala damage. Nat Neurosci. 2013 Mar;16(3):270-2. CrossRef PubMed PubMedCentral
  36. Ziemann A, Allen J, Dahdaleh, Drebot I, Coryell M, Wunsch A, Lynch C, Faraci F, Howard M, Welsh M, Wemmie J. The amygdala is a chemosensor that detects carbon dioxide and acidosis to elicit fear behavior. Cell. 2009 Nov 25;139(5):1012-21. CrossRef PubMed PubMedCentral
  37. Taugher R, Dlouhy B, Kreple C, Ghobbeh A, Conlon M, Wang Y, Wemmie J. The amygdala differentially regulates defensive behaviors evoked by CO2. Behav Brain Res. 2020 Jan 13;377:112236. CrossRef PubMed PubMedCentral
  38. Mir F, Jha S. Locus coeruleus acid-sensing ion channels modulate sleep-wakefulness and state transition from NREM to REM sleep in the rat. Neurosci Bull. 2021 May;37(5):684-700. CrossRef PubMed PubMedCentral
  39. Ghobbeh A, Taugher R, Alam S, Fan R, LaLumiere R, Wemmie A. A novel role for acid-sensing ion channels in Pavlovian reward conditioning. Genes Brain Behav. 2019 Sep;18(7):e12531. CrossRef PubMed PubMedCentral
  40. Bocchio M, Nabavi S, Capogna M. Synaptic plasticity, engrams, and network oscillations in amygdala circuits for storage and retrieval of emotional memories. Neuron. 2017 May 17;94(4):731-43. CrossRef PubMed
  41. Schall T, Wright W, Dong Y. Nucleus accumbens fastspiking interneurons in motivational and addictive behaviors. Mol Psychiatr. 2021 Jan;26(1):234-46. CrossRef PubMed PubMedCentral
  42. Zhang G, Mao L, Wang J, Chu X. Upregulation of acidsensing ion channel 1 protein expression by chronic administration of cocaine in the mouse striatum in vivo. Neurosci Lett. 2009 Aug 14;459(3):119-22. CrossRef PubMed PubMedCentral
  43. Jiang Q, Wang C, Fibuch E, Wang J, Chu X. Differential regulation of locomotor activity to acute and chronic cocaine administration by acid-sensing ion channel 1a and 2 in adult mice. Neuroscience. 2013 Aug 29;246:170-8. CrossRef PubMed PubMedCentral
  44. Gutman A, Cosme C, Noterman M, Worth W, Wemmie J, LaLumiere R. Overexpression of ASIC1A in the nucleus accumbens of rats potentiates cocaine-seeking behavior. Addict Biol. 2020 Mar;25(2):e12690. CrossRef PubMedCentral
  45. Alasmari F, Sari D, Alhaddad H, Al-Rejaie S, Sari Y. Interactive role of acid sensing ion channels and glutamatergic system in opioid dependence. Neurosci Biobehav Rev. 2022 Apr;135:104581. CrossRef PubMed
© National Academy of Sciences of Ukraine, Bogomoletz Institute of Physiology, 2014-2024.