Changes in peripheral HCN2 channels during persistent inflammation

References

• Pinho-Ribeiro FA, Verri WA Jr., Chiu IM. Nociceptor sensory neuron-immune interactions in pain and inflammation. Trends Immunol. 2017 Jan;38(1):5–19.
   PubMed Web of Science ®Google Scholar
• Dubin AE, Patapoutian A. Nociceptors: the sensors of the pain pathway. J Clin Invest. 2010 Nov;120(11):3760–3772.
   PubMed Web of Science ®Google Scholar
• Xu Q, Yaksh TL. A brief comparison of the pathophysiology of inflammatory versus neuropathic pain. Curr Opin Anaesthesiol. 2011 Aug;24(4):400–407.
   PubMed Web of Science ®Google Scholar
• Tsantoulas C, Mooney ER, McNaughton PA. HCN2 ion channels: basic science opens up possibilities for therapeutic intervention in neuropathic pain. Biochem J. 2016 Sept 15;473(18):2717–2736.
   PubMed Web of Science ®Google Scholar
• Emery EC, Young GT, McNaughton PA. HCN2 ion channels: an emerging role as the pacemakers of pain. Trends Pharmacol Sci. 2012 Aug;33(8):456–463.
   PubMed Web of Science ®Google Scholar
• Kuner R, Flor H. Structural plasticity and reorganisation in chronic pain. Nat Rev Neurosci. 2016 Dec 15;18(1):20–30.
   PubMed Web of Science ®Google Scholar
• Du L, Wang SJ, Cui J, et al. Inhibition of HCN channels within the periaqueductal gray attenuates neuropathic pain in rats. Behav Neurosci. 2013 Apr;127(2):325–329.
   PubMed Web of Science ®Google Scholar
• Du L, Wang SJ, Cui J, et al. The role of HCN channels within the periaqueductal gray in neuropathic pain. Brain Res. 2013 Mar;15(1500):36–44.
   Web of Science ®Google Scholar
• Boadas-Vaello P, Homs J, Reina F, et al. Neuroplasticity of supraspinal structures associated with pathological pain. Anat Rec (Hoboken). 2017 Aug;300(8):1481–1501.
   PubMedGoogle Scholar
• Djouhri L, Lawson SN. Abeta-fiber nociceptive primary afferent neurons: a review of incidence and properties in relation to other afferent A-fiber neurons in mammals. Brain Res Brain Res Rev. 2004 Oct;46(2):131–145.
   PubMedGoogle Scholar
• Nagi SS, Marshall AG, Makdani A, et al. An ultrafast system for signaling mechanical pain in human skin. Sci Adv. 2019 July;5(7):eaaw1297.
   PubMed Web of Science ®Google Scholar
• Usoskin D, Furlan A, Islam S, et al. Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat Neurosci. 2015 Jan;18(1):145–153.
   PubMed Web of Science ®Google Scholar
• Li CL, Li KC, Wu D, et al. Somatosensory neuron types identified by high-coverage single-cell RNA-sequencing and functional heterogeneity. Cell Res. 2016 Jan;26(1):83–102.
   PubMed Web of Science ®Google Scholar
• Tibbs GR, Posson DJ, Goldstein PA. Voltage-gated ion channels in the PNS: novel therapies for neuropathic pain? Trends Pharmacol Sci. 2016 July;37(7):522–542.
   PubMed Web of Science ®Google Scholar
• Zemel BM, Ritter DM, Covarrubias M, et al. A-type KV channels in dorsal root ganglion neurons: diversity, function, and dysfunction. Front Mol Neurosci. 2018;11:253.
   PubMed Web of Science ®Google Scholar
• Reichling DB, Levine JD. Critical role of nociceptor plasticity in chronic pain. Trends Neurosci. 2009 Dec;32(12):611–618.
   PubMed Web of Science ®Google Scholar
• Berta T, Qadri Y, Tan PH, et al. Targeting dorsal root ganglia and primary sensory neurons for the treatment of chronic pain. Expert Opin Ther Targets. 2017 July;21(7):695–703.
   PubMed Web of Science ®Google Scholar
• Gold MS, Gebhart GF. Nociceptor sensitization in pain pathogenesis. Nat Med. 2010 Nov;16(11):1248–1257.
   PubMed Web of Science ®Google Scholar
• Pace MC, Passavanti MB, De Nardis L, et al. Nociceptor plasticity: a closer look. J Cell Physiol. 2018 Apr;233(4):2824–2838.
   PubMed Web of Science ®Google Scholar
• Yagi J, Sumino R. Inhibition of a hyperpolarization-activated current by clonidine in rat dorsal root ganglion neurons. J Neurophysiol. 1998 Sept;80(3):1094–1104.
   PubMed Web of Science ®Google Scholar
• Schnorr S, Eberhardt M, Kistner K, et al. HCN2 channels account for mechanical (but not heat) hyperalgesia during long-standing inflammation. Pain. 2014 June;155(6):1079–1090.
   PubMed Web of Science ®Google Scholar
• Emery EC, Young GT, Berrocoso EM, et al. HCN2 ion channels play a central role in inflammatory and neuropathic pain. Science. 2011 Sept 9;333(6048):1462–1466.
   PubMed Web of Science ®Google Scholar
• Takasu K, Ono H, Tanabe M. Spinal hyperpolarization-activated cyclic nucleotide-gated cation channels at primary afferent terminals contribute to chronic pain. Pain. 2010 Oct;151(1):87–96.
   PubMed Web of Science ®Google Scholar
• Wang X, Wang S, Wang W, et al. A novel intrinsic analgesic mechanism: the enhancement of the conduction failure along polymodal nociceptive C-fibers. Pain. 2016 Oct;157(10):2235–2247.
   PubMed Web of Science ®Google Scholar
• Tsantoulas C, Lainez S, Wong S, et al. Hyperpolarization-activated cyclic nucleotide-gated 2 (HCN2) ion channels drive pain in mouse models of diabetic neuropathy. Sci Transl Med. 2017 Sept 27;9(409):eaam6072.
   PubMed Web of Science ®Google Scholar
• Luo L, Chang L, Brown SM, et al. Role of peripheral hyperpolarization-activated cyclic nucleotide-modulated channel pacemaker channels in acute and chronic pain models in the rat. Neuroscience. 2007 Feb 23;144(4):1477–1485.
   PubMed Web of Science ®Google Scholar
• Chaplan SR, Guo HQ, Lee DH, et al. Neuronal hyperpolarization-activated pacemaker channels drive neuropathic pain. J Neurosci. 2003 Feb 15;23(4):1169–1178.
   PubMed Web of Science ®Google Scholar
• Weng X, Smith T, Sathish J, et al. Chronic inflammatory pain is associated with increased excitability and hyperpolarization-activated current (Ih) in C- but not adelta-nociceptors. Pain. 2012 Apr;153(4):900–914.
   PubMed Web of Science ®Google Scholar
• Richards N, Dilley A. Contribution of hyperpolarization-activated channels to heat hypersensitivity and ongoing activity in the neuritis model. Neuroscience. 2015 Jan;22(284):87–98.
   Web of Science ®Google Scholar
• Yao H, Donnelly DF, Ma C, et al. Upregulation of the hyperpolarization-activated cation current after chronic compression of the dorsal root ganglion. J Neurosci. 2003 Mar 15;23(6):2069–2074.
   PubMed Web of Science ®Google Scholar
• Dalle C, Eisenach JC. Peripheral block of the hyperpolarization-activated cation current (Ih) reduces mechanical allodynia in animal models of postoperative and neuropathic pain. Reg Anesth Pain Med. 2005 May–June;30(3):243–248.
   PubMed Web of Science ®Google Scholar
• Sun Q, Xing GG, Tu HY, et al. Inhibition of hyperpolarization-activated current by ZD7288 suppresses ectopic discharges of injured dorsal root ganglion neurons in a rat model of neuropathic pain. Brain Res. 2005 Jan 25;1032(1–2):63–69.
   PubMed Web of Science ®Google Scholar
• Lee DH, Chang L, Sorkin LS, et al. Hyperpolarization-activated, cation-nonselective, cyclic nucleotide-modulated channel blockade alleviates mechanical allodynia and suppresses ectopic discharge in spinal nerve ligated rats. J Pain. 2005 July;6(7):417–424.
   PubMed Web of Science ®Google Scholar
• Huang H, Zhang Z, Huang D. Decreased HCN2 channel expression attenuates neuropathic pain by inhibiting pro-inflammatory reactions and NF-kappaB activation in mice. Int J Clin Exp Pathol. 2019;12(1):154–163.
   PubMed Web of Science ®Google Scholar
• Wahl-Schott C, Biel M. HCN channels: structure, cellular regulation and physiological function. Cell Mol Life Sci. 2009 Feb;66(3):470–494.
   PubMed Web of Science ®Google Scholar
• Sartiani L, Mannaioni G, Masi A, et al. The Hyperpolarization-activated cyclic nucleotide-gated channels: from biophysics to pharmacology of a unique family of ion channels. Pharmacol Rev. 2017 Oct;69(4):354–395.
   PubMed Web of Science ®Google Scholar
• Gao LL, McMullan S, Djouhri L, et al. Expression and properties of hyperpolarization-activated current in rat dorsal root ganglion neurons with known sensory function. J Physiol. 2012 Oct 1;590(19):4691–4705.
   PubMed Web of Science ®Google Scholar
• Kouranova EV, Strassle BW, Ring RH, et al. Hyperpolarization-activated cyclic nucleotide-gated channel mRNA and protein expression in large versus small diameter dorsal root ganglion neurons: correlation with hyperpolarization-activated current gating. Neuroscience. 2008 June 2;153(4):1008–1019.
   PubMed Web of Science ®Google Scholar
• Momin A, Cadiou H, Mason A, et al. Role of the hyperpolarization-activated current Ih in somatosensory neurons. J Physiol. 2008 Dec 15;586(24):5911–5929.
   PubMed Web of Science ®Google Scholar
• Lainez S, Tsantoulas C, Biel M, et al. HCN3 ion channels: roles in sensory neuronal excitability and pain. J Physiol. 2019 Sept;597(17):4661–4675.
   PubMed Web of Science ®Google Scholar
• Dini L, Del Lungo M, Resta F, et al. Selective blockade of HCN1/HCN2 channels as a potential pharmacological strategy against pain. Front Pharmacol. 2018;9:1252.
   PubMed Web of Science ®Google Scholar
• Resta F, Micheli L, Laurino A, et al. Selective HCN1 block as a strategy to control oxaliplatin-induced neuropathy. Neuropharmacology. 2018 Mar 15;131:403–413.
   PubMed Web of Science ®Google Scholar
• Francois-Moutal L, Scott DD, Perez-Miller S, et al. Chemical shift perturbation mapping of the Ubc9-CRMP2 interface identifies a pocket in CRMP2 amenable for allosteric modulation of Nav1.7 channels. Channels (Austin). 2018;12(1):219–227.
   PubMed Web of Science ®Google Scholar
• Moutal A, Yang X, Li W, et al. CRISPR/Cas9 editing of Nf1 gene identifies CRMP2 as a therapeutic target in neurofibromatosis type 1-related pain that is reversed by (S)-Lacosamide. Pain. 2017 Dec;158(12):2301–2319.
   PubMed Web of Science ®Google Scholar
• Djouhri L, Dawbarn D, Robertson A, et al. Time course and nerve growth factor dependence of inflammation-induced alterations in electrophysiological membrane properties in nociceptive primary afferent neurons. J Neurosci. 2001 Nov 15;21(22):8722–8733.
   PubMed Web of Science ®Google Scholar
• Basbaum AI, Bautista DM, Scherrer G, et al. Cellular and molecular mechanisms of pain. Cell. 2009 Oct 16;139(2):267–284.
   PubMed Web of Science ®Google Scholar
• Hucho T, Levine JD. Signaling pathways in sensitization: toward a nociceptor cell biology. Neuron. 2007 Aug 2;55(3):365–376.
   PubMed Web of Science ®Google Scholar
• Cheng JK, Ji RR. Intracellular signaling in primary sensory neurons and persistent pain. Neurochem Res. 2008 Oct;33(10):1970–1978.
   PubMed Web of Science ®Google Scholar
• Acosta C, McMullan S, Djouhri L, et al. HCN1 and HCN2 in Rat DRG neurons: levels in nociceptors and non-nociceptors, NT3-dependence and influence of CFA-induced skin inflammation on HCN2 and NT3 expression. PLoS One. 2012;7(12):e50442.
   PubMed Web of Science ®Google Scholar
• Smith T, Al Otaibi M, Sathish J, et al. Increased expression of HCN2 channel protein in L4 dorsal root ganglion neurons following axotomy of L5- and inflammation of L4-spinal nerves in rats. Neuroscience. 2015 June 4;295:90–102.
   PubMed Web of Science ®Google Scholar
• Papp I, Hollo K, Antal M. Plasticity of hyperpolarization-activated and cyclic nucleotid-gated cation channel subunit 2 expression in the spinal dorsal horn in inflammatory pain. Eur J Neurosci. 2010 Oct;32(7):1193–1201.
   PubMed Web of Science ®Google Scholar
• Jiang YQ, Xing GG, Wang SL, et al. Axonal accumulation of hyperpolarization-activated cyclic nucleotide-gated cation channels contributes to mechanical allodynia after peripheral nerve injury in rat. Pain. 2008 July 31;137(3):495–506.
   PubMed Web of Science ®Google Scholar
• Liu Y, Feng Y, Zhang T. Pulsed radiofrequency treatment enhances dorsal root ganglion expression of hyperpolarization-activated cyclic nucleotide-gated channels in a rat model of neuropathic pain. J Mol Neurosci. 2015 Sept;57(1):97–105.
   PubMed Web of Science ®Google Scholar
• Cho HJ, Staikopoulos V, Furness JB, et al. Inflammation-induced increase in hyperpolarization-activated, cyclic nucleotide-gated channel protein in trigeminal ganglion neurons and the effect of buprenorphine. Neuroscience. 2009 Aug 18;162(2):453–461.
   PubMed Web of Science ®Google Scholar
• Forster LA, Jansen LR, Rubaharan M, et al. Alterations in SUMOylation of the hyperpolarization-activated cyclic nucleotide gated ion channel 2 during persistent inflammation. Eur J Pain. 2020 May 23;24:1517–1536.
   PubMed Web of Science ®Google Scholar
• Li WM, Cui KM, Li N, et al. Analgesic effect of electroacupuncture on complete Freund’s adjuvant-induced inflammatory pain in mice: a model of antipain treatment by acupuncture in mice. Jpn J Physiol. 2005 Dec;55(6):339–344.
   PubMedGoogle Scholar
• Millan MJ, Czlonkowski A, Morris B, et al. Inflammation of the hind limb as a model of unilateral, localized pain: influence on multiple opioid systems in the spinal cord of the rat. Pain. 1988 Dec;35(3):299–312.
   PubMed Web of Science ®Google Scholar
• Taiwo YO, Levine JD. Further confirmation of the role of adenyl cyclase and of cAMP-dependent protein kinase in primary afferent hyperalgesia. Neuroscience. 1991;44(1):131–135.
   PubMed Web of Science ®Google Scholar
• Resta F, Masi A, Sili M, et al. Kynurenic acid and zaprinast induce analgesia by modulating HCN channels through GPR35 activation. Neuropharmacology. 2016 Sept;108:136–143.
   PubMed Web of Science ®Google Scholar
• Malmberg AB, Brandon EP, Idzerda RL, et al. Diminished inflammation and nociceptive pain with preservation of neuropathic pain in mice with a targeted mutation of the type I regulatory subunit of cAMP-dependent protein kinase. J Neurosci. 1997 Oct 1;17(19):7462–7470.
   PubMed Web of Science ®Google Scholar
• Herrmann S, Rajab H, Christ I, et al. Protein kinase A regulates inflammatory pain sensitization by modulating HCN2 channel activity in nociceptive sensory neurons. Pain. 2017 Oct;158(10):2012–2024.
   PubMed Web of Science ®Google Scholar
• Djouhri L, Al Otaibi M, Kahlat K, et al. Persistent hindlimb inflammation induces changes in activation properties of hyperpolarization-activated current (Ih) in rat C-fiber nociceptors in vivo. Neuroscience. 2015 Aug;20(301):121–133.
   Web of Science ®Google Scholar
• Nawathe PA, Kryukova Y, Oren RV, et al. An LQTS6 MiRP1 mutation suppresses pacemaker current and is associated with sinus bradycardia. J Cardiovasc Electrophysiol. 2013 Sept;24(9):1021–1027.
   PubMed Web of Science ®Google Scholar
• Qu J, Kryukova Y, Potapova IA, et al. MiRP1 modulates HCN2 channel expression and gating in cardiac myocytes. J Biol Chem. 2004 Oct 15;279(42):43497–43502.
   PubMed Web of Science ®Google Scholar
• Brandt MC, Endres-Becker J, Zagidullin N, et al. Effects of KCNE2 on HCN isoforms: distinct modulation of membrane expression and single channel properties. Am J Physiol Heart Circ Physiol. 2009 July;297(1):H355–63.
   PubMed Web of Science ®Google Scholar
• Kimura K, Kitano J, Nakajima Y, et al. Hyperpolarization-activated, cyclic nucleotide-gated HCN2 cation channel forms a protein assembly with multiple neuronal scaffold proteins in distinct modes of protein-protein interaction. Genes Cells. 2004 July;9(7):631–640.
   PubMed Web of Science ®Google Scholar
• Santoro B, Wainger BJ, Siegelbaum SA. Regulation of HCN channel surface expression by a novel C-terminal protein-protein interaction. J Neurosci. 2004 Nov 24;24(47):10750–10762.
   PubMed Web of Science ®Google Scholar
• Michels G, Er F, Khan IF, et al. K+ channel regulator KCR1 suppresses heart rhythm by modulating the pacemaker current If. PLoS One. 2008 Jan 30;3(1):e1511.
   PubMed Web of Science ®Google Scholar
• Flotho A, Melchior F. Sumoylation: a regulatory protein modification in health and disease. Annu Rev Biochem. 2013;82:357–385.
   PubMed Web of Science ®Google Scholar
• Hendriks IA, D’Souza RC, Chang JG, et al. System-wide identification of wild-type SUMO-2 conjugation sites. Nat Commun. 2015 June 15;6:7289.
   PubMed Web of Science ®Google Scholar
• Parker AR, Welch MA, Forster LA, et al. SUMOylation of the hyperpolarization-activated cyclic nucleotide-gated channel 2 increases surface expression and the maximal conductance of the hyperpolarization-activated current. Front Mol Neurosci. 2017;9:168.
   PubMed Web of Science ®Google Scholar
• Wang Y, Gao Y, Tian Q, et al. Author correction: TRPV1 SUMOylation regulates nociceptive signaling in models of inflammatory pain. Nat Commun. 2018 June 28;9(1):2593.
   PubMed Web of Science ®Google Scholar
• Dustrude ET, Moutal A, Yang X, et al. Hierarchical CRMP2 posttranslational modifications control NaV1.7 function. Proc Natl Acad Sci U S A. 2016 Dec 27;113(52):E8443–E8452.
   PubMed Web of Science ®Google Scholar
• Parker AR, Forster LA, Baro DJ. Modulator-gated, SUMOylation-mediated, activity-dependent regulation of ionic current densities contributes to short-term activity homeostasis. J Neurosci. 2019 Jan 23;39(4):596–611.
   PubMed Web of Science ®Google Scholar
• Rigaud M, Gemes G, Barabas ME, et al. Species and strain differences in rodent sciatic nerve anatomy: implications for studies of neuropathic pain. Pain. 2008 May;136(1–2):188–201.
   PubMed Web of Science ®Google Scholar
• Swett JE, Torigoe Y, Elie VR, et al. Sensory neurons of the rat sciatic nerve. Exp Neurol. 1991 Oct;114(1):82–103.
   PubMed Web of Science ®Google Scholar
• Salo PT, Theriault E. Number, distribution and neuropeptide content of rat knee joint afferents. J Anat. 1997 May;190(Pt 4):515–522.
   PubMed Web of Science ®Google Scholar
• Nakajima T, Ohtori S, Inoue G, et al. The characteristics of dorsal-root ganglia and sensory innervation of the hip in rats. J Bone Joint Surg Br. 2008 Feb;90(2):254–257.
   PubMedGoogle Scholar
• Herrity AN, Rau KK, Petruska JC, et al. Identification of bladder and colon afferents in the nodose ganglia of male rats. J Comp Neurol. 2014 Nov 1;522(16):3667–3682.
   PubMed Web of Science ®Google Scholar
• Belkouch M, Dansereau MA, Tetreault P, et al. Functional up-regulation of Nav1.8 sodium channel in Abeta afferent fibers subjected to chronic peripheral inflammation. J Neuroinflammation. 2014 Mar 7;11:45.
   PubMed Web of Science ®Google Scholar
• Koltzenburg M, Wall PD, McMahon SB. Does the right side know what the left is doing? Trends Neurosci. 1999 Mar;22(3):122–127.
   PubMed Web of Science ®Google Scholar
• Welch MA, Forster LA, Atlas SI, et al. SUMOylating two distinct sites on the A-type potassium channel, Kv4.2, Increases surface expression and decreases current amplitude [Original Research]. Front Mol Neurosci. 2019 May 31;12(144). DOI:https://doi.org/10.3389/fnmol.2019.00144
   Google Scholar
• Steffensen AB, Andersen MN, Mutsaers N, et al. SUMO co-expression modifies K V 11.1 channel activity. Acta Physiol (Oxf). 2018 Mar;222(3):e12974.
   PubMed Web of Science ®Google Scholar
• Xiong D, Li T, Dai H, et al. SUMOylation determines the voltage required to activate cardiac IKs channels. Proc Natl Acad Sci U S A. 2017 Aug 8;114(32):E6686–E6694.
   PubMed Web of Science ®Google Scholar
• Plant LD, Dementieva IS, Kollewe A, et al. One SUMO is sufficient to silence the dimeric potassium channel K2P1. Proc Natl Acad Sci U S A. 2010 June 8;107(23):10743–10748.
   PubMed Web of Science ®Google Scholar
• Benson MD, Li QJ, Kieckhafer K, et al. SUMO modification regulates inactivation of the voltage-gated potassium channel Kv1.5. Proc Natl Acad Sci U S A. 2007 Feb 6;104(6):1805–1810.
   PubMed Web of Science ®Google Scholar
• Plant LD, Marks JD, Goldstein SA. SUMOylation of NaV1.2 channels mediates the early response to acute hypoxia in central neurons. Elife. 2016 Dec 28;5. DOI:https://doi.org/10.7554/eLife.20054
   Google Scholar
• Dai XQ, Kolic J, Marchi P, et al. SUMOylation regulates Kv2.1 and modulates pancreatic beta-cell excitability. J Cell Sci. 2009 Mar 15;122(Pt6):775–779.
   PubMed Web of Science ®Google Scholar
• Seifert A, Schofield P, Barton GJ, et al. Proteotoxic stress reprograms the chromatin landscape of SUMO modification. Sci Signal. 2015 July 7;8(384):rs7.
   PubMed Web of Science ®Google Scholar
• Dustrude ET, Wilson SM, Ju W, et al. CRMP2 protein SUMOylation modulates NaV1.7 channel trafficking. J Biol Chem. 2013 Aug 23;288(34):24316–24331.
   PubMed Web of Science ®Google Scholar
• Francois-Moutal L, Dustrude ET, Wang Y, et al. Inhibition of the Ubc9 E2 SUMO-conjugating enzyme-CRMP2 interaction decreases NaV1.7 currents and reverses experimental neuropathic pain. Pain. 2018 Oct;159(10):2115–2127.
   PubMed Web of Science ®Google Scholar
• Largent-Milnes TM, Dustrude ET, Largent-Milnes TM, et al. Blocking CRMP2 SUMOylation reverses neuropathic pain. Mol Psychiatry. 2017 May 23;23:1745–1755.
   PubMed Web of Science ®Google Scholar
• Qi Y, Wang J, Bomben VC, et al. Hyper-SUMOylation of the Kv7 potassium channel diminishes the M-current leading to seizures and sudden death. Neuron. 2014 Sept 3;83(5):1159–1171.
   PubMed Web of Science ®Google Scholar
• Plant LD, Dowdell EJ, Dementieva IS, et al. SUMO modification of cell surface Kv2.1 potassium channels regulates the activity of rat hippocampal neurons. J Gen Physiol. 2011 May;137(5):441–454.
   PubMed Web of Science ®Google Scholar
• Rajan S, Plant LD, Rabin ML, et al. Sumoylation silences the plasma membrane leak K+ channel K2P1. Cell. 2005 Apr 8;121(1):37–47.
   PubMed Web of Science ®Google Scholar
• Plant LD, Xiong D, Romero J, et al. Hypoxia produces pro-arrhythmic late sodium current in cardiac myocytes by SUMOylation of NaV1.5 channels. Cell Rep. 2020 Feb 18;30(7):2225–2236e4.
   PubMed Web of Science ®Google Scholar