1,102
Views
3
CrossRef citations to date
0
Altmetric
Review

Nitrergic modulation of ion channel function in regulating neuronal excitability

ORCID Icon & ORCID Icon
Pages 666-679 | Received 11 Sep 2021, Accepted 01 Nov 2021, Published online: 22 Nov 2021

References

  • Caviedes A, Varas-Godoy M, Lafourcade C, et al. Endothelial nitric oxide synthase is present in dendritic spines of neurons in primary cultures. Front Cell Neurosci. 2017;11:180.
  • Bourgognon JM, Spiers JG, Robinson SW, et al. Inhibition of neuroinflammatory nitric oxide signaling suppresses glycation and prevents neuronal dysfunction in mouse prion disease. Proc Natl Acad Sci U S A. 2021;118(10).
  • Berliocchi L, Corasaniti MT, Bagetta G, et al. Neuroinflammation in neuronal degeneration and repair. Cell Death Differ. 2007;14(4):883–884.
  • Bourgognon JM, Steinert JR. The metabolome identity: basis for discovery of biomarkers in neurodegeneration. Neural Regen Res. 2019;14(3):387–390.
  • Steinert JR, Chernova T, Forsythe ID. Nitric oxide signaling in brain function, dysfunction, and dementia. Neuroscientist. 2010;16(4):435–452.
  • Bradley SA, Steinert JR. Nitric oxide-mediated posttranslational modifications: impacts at the synapse. Oxid Med Cell Longev. 2016;2016:5681036.
  • Hardingham N, Dachtler J, Fox K. The role of nitric oxide in pre-synaptic plasticity and homeostasis. Front Cell Neurosci. 2013;7:190.
  • Gamper N, Ooi L. Redox and nitric oxide-mediated regulation of sensory neuron ion channel function. Antioxid Redox Signal. 2015;22(6):486–504.
  • Garthwaite J. Concepts of neural nitric oxide-mediated transmission. Eur J Neurosci. 2008;27:2783–2802.
  • Garthwaite J. NO as a multimodal transmitter in the brain: discovery and current status. Br J Pharmacol. 2019;176(2):197–211.
  • Aso Y, Ray RP, Long X, et al. Nitric oxide acts as a cotransmitter in a subset of dopaminergic neurons to diversify memory dynamics. Elife. 2019;8. DOI:https://doi.org/10.7554/eLife.49257.
  • Robinson SW, Bourgognon JM, Spiers JG, et al. Nitric oxide-mediated posttranslational modifications control neurotransmitter release by modulating complexin farnesylation and enhancing its clamping ability. PLoS Biol. 2018;16(4):e2003611.
  • Goldner A, Farruggella J, Wainwright ML, et al. cGMP mediates short- and long-term modulation of excitability in a decision-making neuron in Aplysia. Neurosci Lett. 2018;683:111–118.
  • Briskin-Luchinsky V, Tam S, Shabbat S, et al. NO is required for memory formation and expression of memory, and for minor behavioral changes during training with inedible food in Aplysia. Learn Mem. 2018;25(5):206–213.
  • Jinno S, Aika Y, Fukuda T, et al. Quantitative analysis of neuronal nitric oxide synthase-immunoreactive neurons in the mouse hippocampus with optical disector. J Comp Neurol. 1999;410(3):398–412.
  • Megias M, Verduga R, Fernandez-Viadero C, et al. Neurons co-localizing calretinin immunoreactivity and reduced nicotinamide adenine dinucleotide phosphate diaphorase (NADPH-d) activity in the hippocampus and dentate gyrus of the rat. Brain Res. 1997;744(1):112–120.
  • Tricoire L, Pelkey KA, Daw MI, et al. Common origins of hippocampal Ivy and nitric oxide synthase expressing neurogliaform cells. J Neurosci. 2010;30(6):2165–2176.
  • Lourenco CF, Ferreira NR, Santos RM, et al. The pattern of glutamate-induced nitric oxide dynamics in vivo and its correlation with nNOS expression in rat hippocampus, cerebral cortex and striatum. Brain Res. 2014;1554:1–11.
  • Lipton SA, Choi YB, Pan ZH, et al. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature. 1993;364(6438):626–632.
  • Beckman JS, Beckman TW, Chen J, et al. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A. 1990;87(4):1620–1624.
  • Bradley SA, Steinert JR. Characterisation and comparison of temporal release profiles of nitric oxide generating donors. J Neurosci Methods. 2015;245:116–124.
  • Chung YH, Kim YS, Lee WB. Distribution of neuronal nitric oxide synthase-immunoreactive neurons in the cerebral cortex and hippocampus during postnatal development. J Mol Histol. 2004;35(8–9):765–770.
  • Steinert JR, Postlethwaite M, Jordan MD, et al. NMDAR-mediated EPSCs are maintained and accelerate in time course during maturation of mouse and rat auditory brainstem in vitro. J Physiol. 2010;588(3):447–463.
  • Philippides A, Ott SR, Husbands P, et al. Modeling cooperative volume signaling in a plexus of nitric-oxide-synthase-expressing neurons. J Neurosci. 2005;25(28):6520–6532.
  • Batchelor AM, Bartus K, Reynell C, et al. Exquisite sensitivity to subsecond, picomolar nitric oxide transients conferred on cells by guanylyl cyclase-coupled receptors. Proc Natl Acad Sci U S A. 2010;107(51):22060–22065.
  • Ledo A, Barbosa R, Cadenas E, et al. Dynamic and interacting profiles of *NO and O2 in rat hippocampal slices. Free Radic Biol Med. 2010;48(8):1044–1050.
  • Ledo A, Barbosa RM, Gerhardt GA, et al. Concentration dynamics of nitric oxide in rat hippocampal subregions evoked by stimulation of the NMDA glutamate receptor. Proc Natl Acad Sci U S A. 2005;102(48):17483–17488.
  • Wood KC, Batchelor AM, Bartus K, et al. Picomolar nitric oxide signals from central neurons recorded using ultrasensitive detector cells. J Biol Chem. 2011;286(50):43172–43181.
  • Brock MW, Mathes C, Gilly WF. Selective open-channel block of Shaker (Kv1) potassium channels by s-nitrosodithiothreitol (SNDTT). J Gen Physiol. 2001;118(1):113–134.
  • Nunez L, Vaquero M, Gomez R, et al. Nitric oxide blocks hKv1.5 channels by S-nitrosylation and by a cyclic GMP-dependent mechanism. Cardiovasc Res. 2006;72(1):80–89.
  • Malinski T. Understanding nitric oxide physiology in the heart: a nanomedical approach. Am J Cardiol. 2005;96(7):13i–24i.
  • Scheiblich H, Steinert JR. Nitrergic modulation of neuronal excitability in the mouse hippocampus is mediated via regulation of Kv2 and voltage-gated sodium channels. Hippocampus. 2021;31(9):1020–1038.
  • Steinert JR, Robinson SW, Tong H, et al. Nitric oxide is an activity-dependent regulator of target neuron intrinsic excitability. Neuron. 2011;71(2):291–305.
  • Holm P, Kankaanranta H, Metsa-Ketela T, et al. Radical releasing properties of nitric oxide donors GEA 3162, SIN-1 and S-nitroso-N-acetylpenicillamine. Eur J Pharmacol. 1998;346(1):97–102.
  • Pal S, He K, Aizenman E. Nitrosative stress and potassium channel-mediated neuronal apoptosis: is zinc the link? Pflugers Arch. 2004;448(3):296–303.
  • Moreno H, Vega-saenz de Miera E, Nadal MS, et al. Modulation of Kv3 potassium channels expressed in CHO cells by a nitric oxide-activated phosphatase. J Physiol. 2001;530(3):345–358.
  • Steinert JR, Kopp-Scheinpflug C, Baker C, et al. Nitric oxide is a volume transmitter regulating postsynaptic excitability at a glutamatergic synapse. Neuron. 2008;60(4):642–656.
  • Cai X, Liang CW, Muralidharan S, et al. Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron. 2004;44(2):351–364.
  • Stuhmer W, Ruppersberg JP, Schroter KH, et al. Molecular basis of functional diversity of voltage-gated potassium channels in mammalian brain. EMBO J. 1989;8(11):3235–3244.
  • Wang G, Strang C, Pfaffinger PJ, et al. Zn2+-dependent redox switch in the intracellular T1-T1 interface of a Kv channel. J Biol Chem. 2007;282(18):13637–13647.
  • Huang H, Trussell LO. KCNQ5 channels control resting properties and release probability of a synapse. Nat Neurosci. 2011;14(7):840–847.
  • Ooi L, Gigout S, Pettinger L, et al. Triple cysteine module within M-type K+ channels mediates reciprocal channel modulation by nitric oxide and reactive oxygen species. J Neurosci. 2013;33(14):6041–6046.
  • Artinian L, Zhong L, Yang H, et al. Nitric oxide as intracellular modulator: internal production of NO increases neuronal excitability via modulation of several ionic conductances. Eur J Neurosci. 2012;36(10):3333–3343.
  • Zhong LR, Estes S, Artinian L, et al. Nitric oxide regulates neuronal activity via calcium-activated potassium channels. PLoS One. 2013;8(11):e78727.
  • Klyachko VA, Ahern GP, Jackson MB. cGMP-mediated facilitation in nerve terminals by enhancement of the spike afterhyperpolarization. Neuron. 2001;31(6):1015–1025.
  • Kyle BD, Hurst S, Swayze RD, et al. Specific phosphorylation sites underlie the stimulation of a large conductance, Ca2+-activated K+ channel by cGMP-dependent protein kinase. FASEB J. 2013;27(5):2027–2038.
  • Tjong YW, Li M, Hung MW, et al. Nitric oxide deficit in chronic intermittent hypoxia impairs large conductance calcium-activated potassium channel activity in rat hippocampal neurons. Free Radic Biol Med. 2008;44(4):547–557.
  • Bock T, Stuart GJ. The impact of BK channels on cellular excitability depends on their subcellular location. Front Cell Neurosci. 2016;10:206.
  • Renganathan M, Cummins TR, Waxman SG. Nitric oxide blocks fast, slow, and persistent Na+ channels in C-type DRG neurons by S-nitrosylation. J Neurophysiol. 2002;87(2):761–775.
  • Hammarstrom AK, Gage PW. Nitric oxide increases persistent sodium current in rat hippocampal neurons. J Physiol. 1999;520(Pt 2):451–461.
  • Ikeda M, Yoshino M. Nitric oxide augments single persistent Na+ channel currents via the cGMP/PKG signaling pathway in Kenyon cells isolated from cricket mushroom bodies. J Neurophysiol. 2018;120(2):720–728.
  • Frere SG, Kuisle M, Luthi A. Regulation of recombinant and native hyperpolarization-activated cation channels. Mol Neurobiol. 2004;30(3):279–305.
  • Byczkowicz N, Eshra A, Montanaro J, et al. HCN channel-mediated neuromodulation can control action potential velocity and fidelity in central axons. Elife. 2019;8. DOI:https://doi.org/10.7554/eLife.42766.
  • Pires Da Silva M, de Almeida Moraes DJ, Mecawi AS, et al. Nitric oxide modulates HCN channels in magnocellular neurons of the supraoptic nucleus of rats by an S-Nitrosylation-dependent mechanism. J Neurosci. 2016;36(44):11320–11330.
  • Almanza A, Navarrete F, Vega R, et al. Modulation of voltage-gated Ca2+ current in vestibular hair cells by nitric oxide. J Neurophysiol. 2007;97(2):1188–1195.
  • Lv P, Rodriguez-Contreras A, Kim HJ, et al. Release and elementary mechanisms of nitric oxide in hair cells. J Neurophysiol. 2010;103(5):2494–2505.
  • Wenker IC, Benoit JP, Chen X, et al. Nitric oxide activates hypoglossal motoneurons by cGMP-dependent inhibition of TASK channels and cGMP-independent activation of HCN channels. J Neurophysiol. 2012;107(5):1489–1499.
  • Xue Y, Liu Z, Gao X, et al. GPS-SNO: computational prediction of protein S-nitrosylation sites with a modified GPS algorithm. PLoS One. 2010;5(6):e11290.
  • Petzold GC, Scheibe F, Braun JS, et al. Nitric oxide modulates calcium entry through P/Q-type calcium channels and N-methyl-d-aspartate receptors in rat cortical neurons. Brain Res. 2005;1063(1):9–14.
  • Dolphin AC. Ca2+ channel currents in rat sensory neurones: interaction between guanine nucleotides, cyclic AMP and Ca2+ channel ligands. J Physiol. 1991;432(1):23–43.
  • Tozer AJ, Forsythe ID, Steinert JR. Nitric oxide signalling augments neuronal voltage-gated L-type (Ca(v)1) and P/q-type (Ca(v)2.1) channels in the mouse medial nucleus of the trapezoid body. PLoS One. 2012;7(2):e32256.
  • Jian K, Chen M, Cao X, et al. Nitric oxide modulation of voltage-gated calcium current by S-nitrosylation and cGMP pathway in cultured rat hippocampal neurons. Biochem Biophys Res Commun. 2007;359(3):481–485.
  • D’Ascenzo M, Martinotti G, Azzena GB, et al. cGMP/Protein Kinase G-dependent inhibition of N-type Ca2+ channels induced by nitric oxide in human neuroblastoma IMR32 cells. J Neurosci. 2002;22(17):7485–7492.
  • Chen J, Daggett H, De Waard M, et al. Nitric oxide augments voltage-gated P/Q-type Ca(2+) channels constituting a putative positive feedback loop. Free Radic Biol Med. 2002;32(7):638–649.
  • Li Q, Zhang Y, Wu N, et al. Activation of somatostatin receptor 5 suppresses T-type Ca(2+) channels through NO/cGMP/PKG signaling pathway in rat retinal ganglion cells. Neurosci Lett. 2019;708:134337.
  • Joksovic PM, Doctor A, Gaston B, et al. Functional regulation of T-type calcium channels by s-nitrosothiols in the rat thalamus. J Neurophysiol. 2007;97(4):2712–2721.
  • Lee J, Nelson MT, Rose KE, et al. Redox mechanism of S-nitrosothiol modulation of neuronal CaV3.2 T-type calcium channels. Mol Neurobiol. 2013;48(2):274–280.
  • West AE, Chen WG, Dalva MB, et al. Calcium regulation of neuronal gene expression. Proc Natl Acad Sci U S A. 2001;98(20):11024–11031.
  • West AE, Griffith EC, Greenberg ME. Regulation of transcription factors by neuronal activity. Nat Rev Neurosci. 2002;3(12):921–931.
  • Seino S. ATP-sensitive potassium channels: a model of heteromultimeric potassium channel/receptor assemblies. Annu Rev Physiol. 1999;61(1):337–362.
  • Nichols CG. KATP channels as molecular sensors of cellular metabolism. Nature. 2006;440(7083):470–476.
  • Chi XX, Jiang X, Nicol GD. ATP-sensitive potassium currents reduce the PGE2-mediated enhancement of excitability in adult rat sensory neurons. Brain Res. 2007;1145:28–40.
  • Yamada K, Inagaki N. Neuroprotection by KATP channels. J Mol Cell Cardiol. 2005;38(6):945–949.
  • Soundarapandian MM, Zhong X, Peng L, et al. Role of K(ATP) channels in protection against neuronal excitatory insults. J Neurochem. 2007;103(5):1721–1729.
  • Brayden JE. Functional roles of KATP channels in vascular smooth muscle. Clin Exp Pharmacol Physiol. 2002;29(4):312–316.
  • Kawano T, Zoga V, Kimura M, et al. Nitric oxide activates ATP-sensitive potassium channels in mammalian sensory neurons: action by direct S-nitrosylation. Mol Pain. 2009;5:12.
  • Soares AC, Duarte ID. Dibutyryl-cyclic GMP induces peripheral antinociception via activation of ATP-sensitive K(+) channels in the rat PGE2-induced hyperalgesic paw. Br J Pharmacol. 2001;134(1):127–131.
  • Soares AC, Leite R, Tatsuo MA, et al. Activation of ATP-sensitive K(+) channels: mechanism of peripheral antinociceptive action of the nitric oxide donor, sodium nitroprusside. Eur J Pharmacol. 2000;400(1):67–71.
  • Cull-Candy S, Brickley S, Farrant M. NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol. 2001;11(3):327–335.
  • Choi YB, Tenneti L, Le DA, et al. Molecular basis of NMDA receptor-coupled ion channel modulation by S-nitrosylation. Nat Neurosci. 2000;3(1):15–21.
  • Takahashi H, Shin Y, Cho SJ, et al. Hypoxia enhances S-nitrosylation-mediated NMDA receptor inhibition via a thiol oxygen sensor motif. Neuron. 2007;53(1):53–64.
  • Qu ZW, Miao WY, Hu SQ, et al. N-methyl-D-aspartate receptor-dependent denitrosylation of neuronal nitric oxide synthase increase the enzyme activity. PLoS One. 2012;7(12):e52788.
  • Wang JQ, Chu XP, Guo ML, et al. Modulation of ionotropic glutamate receptors and Acid-sensing ion channels by nitric oxide. Front Physiol. 2012;3:164.
  • Kakizawa S, Shibazaki M, Mori N. Protein oxidation inhibits NO-mediated signaling pathway for synaptic plasticity. Neurobiol Aging. 2012;33(3):535–545.
  • Huang Y, Man HY, Sekine-Aizawa Y, et al. S-nitrosylation of N-ethylmaleimide sensitive factor mediates surface expression of AMPA receptors. Neuron. 2005;46(4):533–540.
  • Umanah GKE, Ghasemi M, Yin X, et al. AMPA receptor surface expression is regulated by S-Nitrosylation of thorase and transnitrosylation of NSF. Cell Rep. 2020;33(5):108329.
  • Selvakumar B, Jenkins MA, Hussain NK, et al. S-nitrosylation of AMPA receptor GluA1 regulates phosphorylation, single-channel conductance, and endocytosis. Proc Natl Acad Sci U S A. 2013;110(3):1077–1082.
  • Dejanovic B, Schwarz G. Neuronal nitric oxide synthase-dependent S-nitrosylation of gephyrin regulates gephyrin clustering at GABAergic synapses. J Neurosci. 2014;34(23):7763–7768.
  • Kasaragod VB, Schindelin H. Structure-function relationships of glycine and GABAA receptors and their interplay with the scaffolding protein gephyrin. Front Mol Neurosci. 2018;11:317.
  • Gasulla J, Beltran Gonzalez AN, Calvo DJ. Nitric oxide potentiation of the homomeric ρ1 GABAC receptor function. Br J Pharmacol. 2012;167(6):1369–1377.