The Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels: From Biophysics to Pharmacology of a Unique Family of Ion Channels

Sartiani, Laura; Mannaioni, Guido; Masi, Alessio; Novella Romanelli, Maria; Cerbai, Elisabetta

doi:10.1124/pr.117.014035

Cited by 143Ion channel regulation and functionCardiac electrophysiology and arrhythmiasIon Transport and Channel Regulation

The Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels: From Biophysics to Pharmacology of a Unique Family of Ion Channels

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Sartiani, Laura, Mannaioni, Guido, Masi, Alessio, Novella Romanelli, Maria, Cerbai, Elisabetta·2017·Pharmacological Reviews

DOI 10.1124/pr.117.014035

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Abstract

Hyperpolarization-activated, cyclic nucleotide-gated (HCN) channels are important members of the voltage-gated pore loop channels family. They show unique features: they open at hyperpolarizing potential, carry a mixed Na/K current, and are regulated by cyclic nucleotides. Four different isoforms have been cloned (HCN1-4) that can assemble to form homo- or heterotetramers, characterized by different biophysical properties. These proteins are widely distributed throughout the body and involved in different physiologic processes, the most important being the generation of spontaneous electrical activity in the heart and the regulation of synaptic transmission in the brain. Their role in heart rate, neuronal pacemaking, dendritic integration, learning and memory, and visual and pain perceptions has been extensively studied; these channels have been found also in some peripheral tissues, where their functions still need to be fully elucidated. Genetic defects and altered expression of HCN channels are linked to several pathologies, which makes these proteins attractive targets for translational research; at the moment only one drug (ivabradine), which specifically blocks the hyperpolarization-activated current, is clinically available. This review discusses current knowledge about HCN channels, starting from their biophysical properties, origin, and developmental features, to (patho)physiologic role in different tissues and pharmacological modulation, ending with their present and future relevance as drug targets.

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Dysregulated HCN signaling alters resonance and timing, contributing to network states linked to mood and executive symptoms.
“Dysregulated HCN signaling alters resonance and timing, contributing to network states linked to mood and executive symptoms, whereas targeted modulation promises restoration of frequency-specific gain without sacrificing the dynamical flexibility essential for adaptive cognition [272,277].”
From Synaptic Plasticity—Intrinsic Excitability and Antidepressant Discovery (2026) · cites this paper as [277]
The sections on Resonance Properties and Rhythmogenesis say HCN channels shape frequency preference and oscillation timing. The sections on Mood Disorders and Schizophrenia link altered HCN activity to depression-related behavior and impaired prefrontal working memory, respectively. The paper does not establish that altered resonance or timing is the mechanism connecting HCN dysregulation to those mood and executive effects. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Many isoform-preferring HCN tools have incomplete pharmacokinetic and off-target profiling, resulting in narrow therapeutic windows and variable central effects.
“many “isoform-preferring” tools have incomplete pharmacokinetic and off-target profiling, resulting in narrow therapeutic windows and variable central effects [277,298]”
From Synaptic Plasticity—Intrinsic Excitability and Antidepressant Discovery (2026) · cites this paper as [277]
The section “Isoform-Selective HCN Blockers” (page unavailable) describes isoform-preferring compounds and warns that amiodarone’s effects on multiple ion channels may obscure its selectivity. The discussion of HCN blockade also identifies off-target activity and safety concerns for other blockers. Our copy does not establish that many isoform-preferring tools have incomplete pharmacokinetic or off-target profiling, or that this results in narrow therapeutic windows and variable central effects. (LLM, conf=0.83)
Experimental — accuracy not yet measured
In prefrontal cortex, HCN1-driven Ih stabilizes intrinsic persistent firing and supports working memory by maintaining depolarized up-states and filtering distractors within resonant frequency bands.
“In prefrontal cortex, hyperpolarization-activated cyclic nucleotide-gated channel 1 (HCN1)-driven Ih stabilizes intrinsic persistent firing and supports working memory by maintaining depolarized up-states and filtering distractors within resonant frequency bands [275,277,281].”
From Synaptic Plasticity—Intrinsic Excitability and Antidepressant Discovery (2026) · cites this paper as [277]
The section on HCN distribution and function (page unavailable) places HCN1 in prefrontal working-memory circuits and describes HCN current as contributing to neuronal resonance. It does not say that HCN1-driven Ih maintains depolarized up-states or filters distractors to stabilize persistent firing. Instead, it reports that inhibiting cAMP-HCN signaling strengthens recurring prefrontal circuit activity and improves performance, whereas enhanced activity disconnects the network and impairs working memory. (LLM, conf=0.88)
Experimental — accuracy not yet measured
Developmental increases of Ih in pyramidal neurons, along with cell-type-specific regulation by synaptic plasticity and FMRP, refine this gain control and may delineate windows of vulnerability to cognitive dysfunction.
“Developmental increases of Ih in pyramidal neurons, along with cell-type specific regulation by synaptic plasticity and fragile X mental retardation protein (FMRP), refine this gain control and may delineate windows of vulnerability to cognitive dysfunction [277,278,281].”
From Synaptic Plasticity—Intrinsic Excitability and Antidepressant Discovery (2026) · cites this paper as [277]
The “HCN during Organogenesis” section reports a developmental increase in HCN1 expression in rat CA1 pyramidal neurons, while “Synaptic Excitability and Plasticity” describes HCN current shaping synaptic responses and plasticity. Our copy does not establish FMRP regulation of Ih or identify developmental windows of vulnerability to cognitive dysfunction; searches for “FMRP” and “fragile X” found no relevant passage. Page numbers were not available in the indexed passages. (LLM, conf=0.84)
Experimental — accuracy not yet measured
At the network level, HCN4 sustains thalamocortical rhythms that scaffold cortical timing.
“At the network level, hyperpolarization-activated cyclic nucleotide-gated channel 4 (HCN4) sustains thalamocortical rhythms that scaffold cortical timing, linking molecular gating to mesoscale oscillations [272,277,279].”
From Synaptic Plasticity—Intrinsic Excitability and Antidepressant Discovery (2026) · cites this paper as [277]
The “Rhythmogenesis” passage in section B says HCN channels help set the pace of membrane oscillations and influence thalamocortical firing. But it attributes thalamocortical HCN current mainly to HCN2, not HCN4, and does not establish that HCN4 sustains thalamocortical rhythms or scaffolds cortical timing. Page numbers were not available in our copy. (LLM, conf=0.87)
Experimental — accuracy not yet measured

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Mistrík, P., Mader, R. M., Michalakis, S., Weidinger, M., Pfeifer, A., & Biel, M. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m502696200 · Cited by 131 · see citing works
Tetramerization Dynamics of C-terminal Domain Underlies Isoform-specific cAMP Gating in Hyperpolarization-activated Cyclic Nucleotide-gated Channels
Lolicato, M., Nardini, M., Gazzarrini, S., Möller, S., Bertinetti, D., Herberg, F. W., Bolognesi, M., Martin, H., Fasolini, M., Bertrand, J. A., et al. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.297606 · Cited by 130 · see citing works
MiRP1 Modulates HCN2 Channel Expression and Gating in Cardiac Myocytes
Qu, J., Kryukova, Y. N., Potapova, I. A., Doronin, S. V., Larsen, M., Krishnamurthy, G., Cohen, I. S., & Robinson, R. B. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405018200 · Cited by 129 · see citing works
Dual allosteric modulation of pacemaker (f) channels by cAMP and voltage in rabbit SA node
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A Mutant KcsA K+ Channel with Altered Conduction Properties and Selectivity Filter Ion Distribution
Zhou, M., & MacKinnon, R. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.03.020 · Cited by 128 · see citing works
Control of heart rate by cAMP sensitivity of HCN channels
Alig, J., Marger, L., Mesirca, P., Ehmke, H., Mangoni, M. E., & Isbrandt, D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810332106 · Cited by 127 · see citing works
Bradycardic and Proarrhythmic Properties of Sinus Node Inhibitors
Stieber, J., Wieland, K., Stöckl, G., Ludwig, A., & Hofmann, F. B. (2005) · Molecular Pharmacology · doi:10.1124/mol.105.020701 · Cited by 127 · see citing works
Electrophysiological remodeling in heart failure
Wang, Y., & Hill, J. A. (2010) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2010.01.009 · Cited by 126 · see citing works
Activity-Dependent Regulation of HCN Pacemaker Channels by Cyclic AMP
Wang, J., Chen, S., Nolan, M. F., & Siegelbaum, S. A. (2002) · Neuron · doi:10.1016/s0896-6273(02)00968-6 · Cited by 125 · see citing works
The Properties of the Pacemaker Current IFin Human Ventricular Myocytes are Modulated by Cardiac Disease
Cerbai, E., Sartiani, L., DePaoli, P., Pino, R., Maccherini, M., Bizzarri, F., Diciolla, F., Davoli, G., Sani, G., & Mugelli, A. (2001) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.2000.1316 · Cited by 125 · see citing works
Self-citation
Computational analysis of the human sinus node action potential: model development and effects of mutations
Fabbri, A., Fantini, M., Wilders, R., & Severi, S. (2017) · The Journal of Physiology · doi:10.1113/jp273259 · Cited by 125 · see citing works
Inflammatory and neuropathic pain are rapidly suppressed by peripheral block of hyperpolarisation-activated cyclic nucleotide-gated ion channels
Young, G. T., Emery, E. C., Mooney, E. R., Tsantoulas, C., & McNaughton, P. A. (2014) · Pain · doi:10.1016/j.pain.2014.05.021 · Cited by 124 · see citing works
Deletion of the Hyperpolarization-Activated Cyclic Nucleotide-Gated Channel Auxiliary Subunit TRIP8b Impairs HippocampalIhLocalization and Function and Promotes Antidepressant Behavior in Mice
Lewis, A. S., Vaidya, S. P., Blaiss, C. A., Liu, Z., Stoub, T. R., Brager, D. H., Chen, X., Bender, R. A., Estep, C. M., Popov, A. B., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0936-11.2011 · Cited by 123 · see citing works
Hyperpolarization-Activated Current Ih Disconnects Somatic and Dendritic Spike Initiation Zones in Layer V Pyramidal Neurons
Berger, T. K., Senn, W., & Lüscher, H. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00377.2003 · Cited by 122 · see citing works
Dysfunctional HCN ion channels in neurological diseases
DiFrancesco, J. C., & DiFrancesco, D. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00071 · Cited by 121 · see citing works
α2‐Noradrenergic receptors activation enhances excitability and synaptic integration in rat prefrontal cortex pyramidal neurons via inhibition of HCN currents
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Knock-Out of HCN1 Subunit Flattens Dorsal-Ventral Frequency Gradient of Medial Entorhinal Neurons in Adult Mice
Giocomo, L. M., & Hasselmo, M. E. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0609-09.2009 · Cited by 119 · see citing works
Modulation of microglia can attenuate neuropathic pain symptoms and enhance morphine effectiveness
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HCN2 ion channels: an emerging role as the pacemakers of pain
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Dysfunction of Cortical Dendritic Integration in Neuropathic Pain Reversed by Serotoninergic Neuromodulation
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Differential and age-dependent expression of hyperpolarization-activated, cyclic nucleotide-gated cation channel isoforms 1–4 suggests evolving roles in the developing rat hippocampus
Bender, R. A., Brewster, A. L., Santoro, B., Ludwig, A., Hofmann, F. B., Biel, M., & Baram, T. Z. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00314-1 · Cited by 117 · see citing works
Corticospinal-specific HCN expression in mouse motor cortex: Ih-dependent synaptic integration as a candidate microcircuit mechanism involved in motor control
Sheets, P. L., Suter, B. A., Kiritani, T., Chan, C. S., Surmeier, D. J., & Shepherd, G. M. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00232.2011 · Cited by 117 · see citing works
Gabapentin Increases the Hyperpolarization‐activated Cation Current Ih in Rat CA1 Pyramidal Cells
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Augmented currents of an HCN2 variant in patients with febrile seizure syndromes
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Erratum: Timing of cochlear feedback: spatial and temporal representation of a tone across the basilar membrane
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Topographic organization in the auditory brainstem of juvenile mice is disrupted in congenital deafness
Leão, R. N., Sun, H. Q., Leão, K. E., Berntson, A., Youssoufian, M., Paolini, A. G., Fyffe, R. E. W., & Walmsley, B. D. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.098780 · Cited by 111 · see citing works
Modulation of h-Channels in Hippocampal Pyramidal Neurons by p38 Mitogen-Activated Protein Kinase
Poolos, N. P., Bullis, J. B., & Roth, M. K. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2069-06.2006 · Cited by 109 · see citing works
Interaction of the Pacemaker Channel HCN1 with Filamin A
Gravante, B., Barbuti, A., Milanesi, R., Zappi, I., Viscomi, C. F., & DiFrancesco, D. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m401598200 · Cited by 108 · see citing works
Gating of HCN Channels by Cyclic Nucleotides: Residue Contacts that Underlie Ligand Binding, Selectivity, and Efficacy
Zhou, L., & Siegelbaum, S. A. (2007) · Structure · doi:10.1016/j.str.2007.04.012 · Cited by 108 · see citing works
The Role of HCN Channels on Membrane Excitability in the Nervous System
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Modulation of cyclic nucleotide-regulated HCN channels by PIP2 and receptors coupled to phospholipase C
Pian, P., Bucchi, A., DeCostanzo, A. J., Robinson, R. B., & Siegelbaum, S. A. (2007) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-007-0295-2 · Cited by 107 · see citing works
Sick sinus syndrome and atrial fibrillation in older persons — A view from the sinoatrial nodal myocyte
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A Novel Mechanism of Modulation of Hyperpolarization-activated Cyclic Nucleotide-gated Channels by Src Kinase
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Pacemaker Channels and Sinus Node Arrhythmia
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Axonal accumulation of hyperpolarization-activated cyclic nucleotide-gated cation channels contributes to mechanical allodynia after peripheral nerve injury in rat
Jiang, Y., Xing, G., Wang, S.-L., Tu, H., Chi, Y.-N., Li, J., Liu, F., Han, J., & Wan, Y. (2008) · Pain · doi:10.1016/j.pain.2007.10.011 · Cited by 106 · see citing works
Regional distribution of hyperpolarization‐activated current (If) and hyperpolarization‐activated cyclic nucleotide‐gated channel mRNA expression in ventricular cells from control and hypertrophied rat hearts
Fernández‐Velasco, M., Goren, N., Benito, G., Blanco‐Rivero, J., Boscá, L., & Delgado, C. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.041954 · Cited by 105 · see citing works
Localization of f-channels to caveolae mediates specific beta2-adrenergic receptor modulation of rate in sinoatrial myocytes.
Barbuti, A., Terragni, B., Brioschi, C., & DiFrancesco, D. (2007) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2006.09.018 · Cited by 104 · see citing works
Role of peripheral hyperpolarization-activated cyclic nucleotide-modulated channel pacemaker channels in acute and chronic pain models in the rat
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Serious workings of the funny current
DiFrancesco, D. (2005) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2005.05.001 · Cited by 103 · see citing works
Expression of Functional Tyrosine Kinase B Receptors by Rhythmically Active Respiratory Neurons in the Pre-Bötzinger Complex of Neonatal Mice
Thoby‐Brisson, M., Cauli, B., Champagnat, J., Fortin, G., & Katz, D. M. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-20-07685.2003 · Cited by 102 · see citing works
Imidazoline antagonists of α2‐adrenoceptors increase insulin release in vitro by inhibiting ATP‐sensitive K+ channels in pancreatic β‐cells
Jonas, J., Plant, T., & Henquin, J. (1992) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.1992.tb14456.x · Cited by 101 · see citing works

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Etiology and Pharmacology of Neuropathic Pain
Alles, S. R. A., & Smith, P. A. (2018) · Pharmacological Reviews · doi:10.1124/pr.117.014399 · Cited by 395 · see citing works
The Concise Guide to PHARMACOLOGY 2023/24: Ion channels
Alexander, S. P. H., Mathie, A. A., Peters, J. A., Veale, E. L., Striessnig, J., Kelly, E., Armstrong, J. F., Faccenda, E., Harding, S. D., Davies, J. A., et al. (2023) · British Journal of Pharmacology · doi:10.1111/bph.16178 · Cited by 201 · see citing works
Voltage Sensor Movements during Hyperpolarization in the HCN Channel
Lee, C., & MacKinnon, R. (2019) · Cell · doi:10.1016/j.cell.2019.11.006 · Cited by 127 · see citing works
Ih from synapses to networks: HCN channel functions and modulation in neurons
Combe, C. L., & Gasparini, S. (2021) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2021.06.002 · Cited by 101 · see citing works
Cardiac and neuronal HCN channelopathies
Rivolta, I., Binda, A., Masi, A., & DiFrancesco, J. C. (2020) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-020-02384-3 · Cited by 90 · see citing works
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Peripheral Voltage-Gated Cation Channels in Neuropathic Pain and Their Potential as Therapeutic Targets
Alles, S. R. A., & Smith, P. A. (2021) · Frontiers in Pain Research · doi:10.3389/fpain.2021.750583 · Cited by 89 · see citing works
Voltage-sensor movements in the Eag Kv channel under an applied electric field
Mandala, V. S., & MacKinnon, R. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2214151119 · Cited by 87 · see citing works
Selective HCN1 block as a strategy to control oxaliplatin-induced neuropathy
Resta, F., Micheli, L., Laurino, A., Spinelli, V., Mello, T., Sartiani, L., Mannelli, L. D. C., Cerbai, E., Ghelardini, C., Romanelli, M. N., et al. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.01.014 · Cited by 65 · see citing works
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Role of cyclic nucleotides and their downstream signaling cascades in memory function: Being at the right time at the right spot
Argyrousi, E. K., Heckman, P. R. A., & Prickaerts, J. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.02.004 · Cited by 64 · see citing works
Selective Blockade of HCN1/HCN2 Channels as a Potential Pharmacological Strategy Against Pain
Dini, L., Del Lungo, M., Resta, F., Melchiorre, M., Spinelli, V., Di Cesare Mannelli, L., Ghelardini, C., Laurino, A., Sartiani, L., Coppini, R., et al. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.01252 · Cited by 55 · see citing works
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Neuronal hyperexcitability is a DLK-dependent trigger of herpes simplex virus reactivation that can be induced by IL-1
Cuddy, S. R., Schinlever, A. R., Dochnal, S. A., Seegren, P. V., Suzich, J. B., Kundu, P., Downs, T. K., Farah, M., Desai, B. N., Boutell, C., et al. (2020) · eLife · doi:10.7554/elife.58037 · Cited by 55 · see citing works
Gating mechanism of hyperpolarization-activated HCN pacemaker channels
Ramentol, R., Perez, M. E., & Larsson, H. P. (2020) · Nature Communications · doi:10.1038/s41467-020-15233-9 · Cited by 48 · see citing works
The Contribution of HCN Channelopathies in Different Epileptic Syndromes, Mechanisms, Modulators, and Potential Treatment Targets: A Systematic Review
Kessi, M., Peng, J., Duan, H., He, H., Chen, B., Xiong, J., Wang, Y. X., Yang, L., Wang, G., Kiprotich, K., et al. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.807202 · Cited by 43 · see citing works
The Epac1 Protein: Pharmacological Modulators, Cardiac Signalosome and Pathophysiology
Bouvet, M., Blondeau, J., & Lezoualc’h, F. (2019) · Cells · doi:10.3390/cells8121543 · Cited by 41 · see citing works
Oligodendrocyte HCN2 Channels Regulate Myelin Sheath Length
Swire, M., Assinck, P., McNaughton, P. A., Lyons, D. A., ffrench‐Constant, C., & Livesey, M. R. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2463-20.2021 · Cited by 41 · see citing works
A detailed characterization of the hyperpolarization-activated “funny” current (If) in human-induced pluripotent stem cell (iPSC)–derived cardiomyocytes with pacemaker activity
Giannetti, F., Benzoni, P., Campostrini, G., Milanesi, R., Bucchi, A., Baruscotti, M., Dell’Era, P., Rossini, A., & Barbuti, A. (2021) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-021-02571-w · Cited by 39 · see citing works
Molecular and Functional Characterization of Neurogenin-2 Induced Human Sensory Neurons
Hulme, A. E., McArthur, J. R., Maksour, S., Miellet, S., Ooi, L., Adams, D. J., Finol‐Urdaneta, R. K., & Dottori, M. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.600895 · Cited by 34 · see citing works
Pro-Arrhythmic Signaling of Thyroid Hormones and Its Relevance in Subclinical Hyperthyroidism
Tribulová, N., Kurahara, L. H., Hlivák, P., Hirano, K., & Bačová, B. S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21082844 · Cited by 32 · see citing works
Engineering Adenylate Cyclase Activated by Near-Infrared Window Light for Mammalian Optogenetic Applications
Fomicheva, A., Zhou, C., Sun, Q., & Gomelsky, M. (2019) · ACS Synthetic Biology · doi:10.1021/acssynbio.8b00528 · Cited by 28 · see citing works
Painful diabetic neuropathy: The role of ion channels
Wang, Q., Ye, Y., Yang, L., Xiao, L., Liu, J., Zhang, W., & Du, G. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.116417 · Cited by 27 · see citing works
Ion Channel Genes in Painful Neuropathies
Ślęczkowska, M., Misra, K., Santoro, S., Gerrits, M. M., & Hoeijmakers, J. G. J. (2023) · Biomedicines · doi:10.3390/biomedicines11102680 · Cited by 27 · see citing works
Hyperpolarization-activated cyclic-nucleotide-gated channels: pathophysiological, developmental, and pharmacological insights into their function in cellular excitability
Spinelli, V., Sartiani, L., Mugelli, A., Romanelli, M. N., & Cerbai, E. (2018) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2018-0115 · Cited by 26 · see citing works
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Concerted suppression of Ih and activation of IK(M) by ivabradine, an HCN-channel inhibitor, in pituitary cells and hippocampal neurons
Hsiao, H., Liu, Y., Liu, P., & Wu, S. (2019) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2019.03.016 · Cited by 26 · see citing works
Therapeutic Use and Molecular Aspects of Ivabradine in Cardiac Remodeling: A Review
Kamisah, Y., & Hassan, H. H. C. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032801 · Cited by 26 · see citing works
The structure and function of TRIP8b, an auxiliary subunit of hyperpolarization-activated cyclic-nucleotide gated channels
Han, Y. S., Lyman, K. A., Foote, K. M., & Chetkovich, D. M. (2020) · Channels · doi:10.1080/19336950.2020.1740501 · Cited by 25 · see citing works
Functional coupling of Tmem74 and HCN1 channels regulates anxiety-like behavior in BLA neurons
Shao, L.-X., Jiang, Q., Liu, X., Gong, D.-M., Yin, Y., Wu, G., Sun, N.-H., Wang, C.-K., Chen, Q., Yu, C., et al. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0402-8 · Cited by 23 · see citing works
Using a Multiplex Nucleic Acid in situ Hybridization Technique to Determine HCN4 mRNA Expression in the Adult Rodent Brain
Oyrer, J., Bleakley, L. E., Richards, K., Maljevic, S., Phillips, A. M., Petrou, S., Nowell, C. J., & Reid, C. A. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00211 · Cited by 24 · see citing works
Neurofibromatosis type 1 as a model system to study molecular mechanisms of autism spectrum disorder symptoms
Molosh, A. I., & Shekhar, A. (2018) · Progress in brain research · doi:10.1016/bs.pbr.2018.09.014 · Cited by 22 · see citing works
Blockade of HCN2 Channels Provides Neuroprotection Against Ischemic Injury via Accelerating Autophagic Degradation in Hippocampal Neurons
Chen, C., Liu, L., Shu, Y.-Q., Jing, P., Lu, Y., Zhang, X., Zong, X., Guo, L., & Li, C.-J. (2020) · Neuroscience Bulletin · doi:10.1007/s12264-020-00513-7 · Cited by 22 · see citing works
The HCN channel as a pharmacological target: Why, where, and how to block it
Balducci, V., Credi, C., Sacconi, L., Romanelli, M. N., Sartiani, L., & Cerbai, E. (2021) · Progress in Biophysics and Molecular Biology · doi:10.1016/j.pbiomolbio.2021.07.010 · Cited by 21 · see citing works
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Phosphodiesterase 7 as a therapeutic target – Where are we now?
Zorn, A., & Baillie, G. S. (2023) · Cellular Signalling · doi:10.1016/j.cellsig.2023.110689 · Cited by 21 · see citing works
Locally injected ivabradine inhibits carrageenan-induced pain and inflammatory responses via hyperpolarization-activated cyclic nucleotide-gated (HCN) channels
Miyake, S., Higuchi, H., Honda-Wakasugi, Y., Fujimoto, M., Kawai, H., Nagatsuka, H., Maeda, S., & Miyawaki, T. (2019) · PLoS ONE · doi:10.1371/journal.pone.0217209 · Cited by 21 · see citing works
Role of Ion Channels in Alzheimer’s Disease Pathophysiology
Bhoi, R., Mitra, T., Tejaswi, K., Manoj, V., & Ghatak, S. (2025) · The Journal of Membrane Biology · doi:10.1007/s00232-025-00341-8 · Cited by 19 · see citing works
Gene mutations in comorbidity of epilepsy and arrhythmia
Yu, C. J., Deng, X., & Xu, D. (2022) · Journal of Neurology · doi:10.1007/s00415-022-11430-2 · Cited by 19 · see citing works
The hyperpolarization‐activated cyclic nucleotide‐gated 4 channel as a potential anti‐seizure drug target
Kharouf, Q., Phillips, A. M., Bleakley, L. E., Morrisroe, E., Oyrer, J., Jia, L., Ludwig, A., Jin, L., Nicolazzo, J. A., Cerbai, E., et al. (2020) · British Journal of Pharmacology · doi:10.1111/bph.15088 · Cited by 19 · see citing works
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HCN channels in the mammalian cochlea: Expression pattern, subcellular location, and age‐dependent changes
Luque, M., Schrott‐Fischer, A., Dudás, J., Pechriggl, E. J., Brenner, E., Rask‐Andersen, H., Liu, W., & Glueckert, R. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24754 · Cited by 19 · see citing works
Up-regulation of HCN2 channels in a thalamocortical circuit mediates allodynia in mice
Yu, J., Hu, R. M., Mao, Y., Tai, Y., Qun, S., Zhang, Z., Chen, D., & Jin, Y. (2022) · National Science Review · doi:10.1093/nsr/nwac275 · Cited by 19 · see citing works
HCN1 hyperpolarization-activated cyclic nucleotide–gated channels enhance evoked GABA release from parvalbumin-positive interneurons
Buss, E. W., Lofaro, O. M., Barnett, A., Leroy, F., Santoro, B., Siegelbaum, S. A., & Bock, T. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2319246121 · Cited by 18 · see citing works
Central Role of Subthreshold Currents in Myotonia
Metzger, S., Dupont, C., Voss, A. A., & Rich, M. M. (2019) · Annals of Neurology · doi:10.1002/ana.25646 · Cited by 17 · see citing works
Focus on Causality in ESC/iPSC-Based Modeling of Psychiatric Disorders
Hoffmann, A., Ziller, M. J., & Spengler, D. (2020) · Cells · doi:10.3390/cells9020366 · Cited by 17 · see citing works
Effects of Axonal Demyelination, Inflammatory Cytokines and Divalent Cation Chelators on Thalamic HCN Channels and Oscillatory Bursting
Oniani, T., Vinnenberg, L., Chaudhary, R., Schreiber, J. A., Riske, K., Williams, B., Pape, H., White, J. A., Junker, A., Seebohm, G., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23116285 · Cited by 17 · see citing works
Inhibition of hyperpolarization‐activated cyclic nucleotide‐gated channels by β‐blocker carvedilol
Cao, Y., Chen, S., Liang, Y., Wu, T., Pang, J., Liu, S., & Zhou, P. (2018) · British Journal of Pharmacology · doi:10.1111/bph.14469 · Cited by 17 · see citing works
EC18 as a Tool To Understand the Role of HCN4 Channels in Mediating Hyperpolarization-Activated Current in Tissues
Romanelli, M. N., Lungo, M. D., Guandalini, L., Zobeiri, M., Gyökeres, A., Árpádffy‐Lovas, T., Koncz, I., Sartiani, L., Bartolucci, G., Dei, S., et al. (2019) · ACS Medicinal Chemistry Letters · doi:10.1021/acsmedchemlett.8b00587 · Cited by 16 · see citing works
Self-citation
Cardiac K+ Channels and Channelopathies.
Schreiber, J., & Seebohm, G. (2021) · Handbook of Experimental Pharmacology · doi:10.1007/164_2021_513 · Cited by 8 · see citing works
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Authors: Sartiani, L., Mannaioni, G., Masi, A., Novella Romanelli, M., & Cerbai, E.
Affiliations: University of Florence (IT)
ORCID: Sartiani, Laura
Mannaioni, Guido
Masi, Alessio
Cerbai, Elisabetta
Venue: Pharmacological Reviews
Publisher: Elsevier BV
Published: 2017-10
Volume: 69
Issue: 4
Pages: 354-395
ISSN: 0031-6997 (ISSN-L)
DOI: 10.1124/pr.117.014035
OpenAlex: W2753738702
Cited by: 143
References: 497
Citations by year: 2026: 9 · 2025: 17 · 2024: 21 · 2023: 12 · 2022: 19 · 2021: 17 · 2020: 21 · 2019: 16 · 2018: 11
FWCI: 1.23
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
Locations: Pharmacological Reviews (publishedVersion)
PubMed (publishedVersion)
Florence Research (University of Florence) (submittedVersion)
Funders: Ente Cassa di Risparmio di Firenze
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
Keywords: HCN channels, channel biophysics, channel development, cardiac pacemaking, synaptic transmission, heart rate, therapeutic target, ivabradine, channelopathies
MeSH terms: Animals, Biophysics, Humans, Ligands, Nucleotides, Cyclic, Structure-Activity Relationship, Molecular Targeted Therapy, Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels

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The Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels: From Biophysics to Pharmacology of a Unique Family of Ion Channels

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