HCN channels in the mammalian cochlea: Expression pattern, subcellular location, and age‐dependent changes
Neuronal diversity in the cochlea is largely determined by ion channels. Among voltage‐gated channels, hyperpolarization‐activated cyclic nucleotide‐gated (HCN) channels open with hyperpolarization and depolarize the cell until the resting membrane potential. The functions for hearing are not well e...
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| Published in | Journal of neuroscience research Vol. 99; no. 2; pp. 699 - 728 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
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United States
Wiley Subscription Services, Inc
01.02.2021
John Wiley and Sons Inc |
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| Online Access | Get full text |
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| Abstract | Neuronal diversity in the cochlea is largely determined by ion channels. Among voltage‐gated channels, hyperpolarization‐activated cyclic nucleotide‐gated (HCN) channels open with hyperpolarization and depolarize the cell until the resting membrane potential. The functions for hearing are not well elucidated and knowledge about localization is controversial. We created a detailed map of subcellular location and co‐expression of all four HCN subunits across different mammalian species including CBA/J, C57Bl/6N, Ly5.1 mice, guinea pigs, cats, and human subjects. We correlated age‐related hearing deterioration in CBA/J and C57Bl/6N with expression levels of HCN1, −2, and −4 in individual auditory neurons from the same cohort. Spatiotemporal expression during murine postnatal development exposed HCN2 and HCN4 involvement in a critical phase of hair cell innervation. The huge diversity of subunit composition, but lack of relevant heteromeric pairing along the perisomatic membrane and axon initial segments, highlighted an active role for auditory neurons. Neuron clusters were found to be the hot spots of HCN1, −2, and −4 immunostaining. HCN channels were also located in afferent and efferent fibers of the sensory epithelium. Age‐related changes on HCN subtype expression were not uniform among mice and could not be directly correlated with audiometric data. The oldest mice groups revealed HCN channel up‐ or downregulation, depending on the mouse strain. The unexpected involvement of HCN channels in outer hair cell function where HCN3 overlaps prestin location emphasized the importance for auditory function. A better understanding may open up new possibilities to tune neuronal responses evoked through electrical stimulation by cochlear implants.
All HCN channel subtypes were located at subcellular level in human and compared with other mammals such as guinea pig, cat, and three mouse strains. Changes in HCN expression levels were quantified in aging mice and murine postnatal development. The widespread expression and distinct localization emphasized the importance of HCN channels for sound coding and electrical stimulation with cochlear implants |
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| AbstractList | Neuronal diversity in the cochlea is largely determined by ion channels. Among voltage‐gated channels, hyperpolarization‐activated cyclic nucleotide‐gated (HCN) channels open with hyperpolarization and depolarize the cell until the resting membrane potential. The functions for hearing are not well elucidated and knowledge about localization is controversial. We created a detailed map of subcellular location and co‐expression of all four HCN subunits across different mammalian species including CBA/J, C57Bl/6N, Ly5.1 mice, guinea pigs, cats, and human subjects. We correlated age‐related hearing deterioration in CBA/J and C57Bl/6N with expression levels of HCN1, −2, and −4 in individual auditory neurons from the same cohort. Spatiotemporal expression during murine postnatal development exposed HCN2 and HCN4 involvement in a critical phase of hair cell innervation. The huge diversity of subunit composition, but lack of relevant heteromeric pairing along the perisomatic membrane and axon initial segments, highlighted an active role for auditory neurons. Neuron clusters were found to be the hot spots of HCN1, −2, and −4 immunostaining. HCN channels were also located in afferent and efferent fibers of the sensory epithelium. Age‐related changes on HCN subtype expression were not uniform among mice and could not be directly correlated with audiometric data. The oldest mice groups revealed HCN channel up‐ or downregulation, depending on the mouse strain. The unexpected involvement of HCN channels in outer hair cell function where HCN3 overlaps prestin location emphasized the importance for auditory function. A better understanding may open up new possibilities to tune neuronal responses evoked through electrical stimulation by cochlear implants.
All HCN channel subtypes were located at subcellular level in human and compared with other mammals such as guinea pig, cat, and three mouse strains. Changes in HCN expression levels were quantified in aging mice and murine postnatal development. The widespread expression and distinct localization emphasized the importance of HCN channels for sound coding and electrical stimulation with cochlear implants Neuronal diversity in the cochlea is largely determined by ion channels. Among voltage-gated channels, hyperpolarization-activated cyclic nucleotide-gated (HCN) channels open with hyperpolarization and depolarize the cell until the resting membrane potential. The functions for hearing are not well elucidated and knowledge about localization is controversial. We created a detailed map of subcellular location and co-expression of all four HCN subunits across different mammalian species including CBA/J, C57Bl/6N, Ly5.1 mice, guinea pigs, cats, and human subjects. We correlated age-related hearing deterioration in CBA/J and C57Bl/6N with expression levels of HCN1, -2, and -4 in individual auditory neurons from the same cohort. Spatiotemporal expression during murine postnatal development exposed HCN2 and HCN4 involvement in a critical phase of hair cell innervation. The huge diversity of subunit composition, but lack of relevant heteromeric pairing along the perisomatic membrane and axon initial segments, highlighted an active role for auditory neurons. Neuron clusters were found to be the hot spots of HCN1, -2, and -4 immunostaining. HCN channels were also located in afferent and efferent fibers of the sensory epithelium. Age-related changes on HCN subtype expression were not uniform among mice and could not be directly correlated with audiometric data. The oldest mice groups revealed HCN channel up- or downregulation, depending on the mouse strain. The unexpected involvement of HCN channels in outer hair cell function where HCN3 overlaps prestin location emphasized the importance for auditory function. A better understanding may open up new possibilities to tune neuronal responses evoked through electrical stimulation by cochlear implants. Neuronal diversity in the cochlea is largely determined by ion channels. Among voltage-gated channels, hyperpolarization-activated cyclic nucleotide-gated (HCN) channels open with hyperpolarization and depolarize the cell until the resting membrane potential. The functions for hearing are not well elucidated and knowledge about localization is controversial. We created a detailed map of subcellular location and co-expression of all four HCN subunits across different mammalian species including CBA/J, C57Bl/6N, Ly5.1 mice, guinea pigs, cats, and human subjects. We correlated age-related hearing deterioration in CBA/J and C57Bl/6N with expression levels of HCN1, -2, and -4 in individual auditory neurons from the same cohort. Spatiotemporal expression during murine postnatal development exposed HCN2 and HCN4 involvement in a critical phase of hair cell innervation. The huge diversity of subunit composition, but lack of relevant heteromeric pairing along the perisomatic membrane and axon initial segments, highlighted an active role for auditory neurons. Neuron clusters were found to be the hot spots of HCN1, -2, and -4 immunostaining. HCN channels were also located in afferent and efferent fibers of the sensory epithelium. Age-related changes on HCN subtype expression were not uniform among mice and could not be directly correlated with audiometric data. The oldest mice groups revealed HCN channel up- or downregulation, depending on the mouse strain. The unexpected involvement of HCN channels in outer hair cell function where HCN3 overlaps prestin location emphasized the importance for auditory function. A better understanding may open up new possibilities to tune neuronal responses evoked through electrical stimulation by cochlear implants.Neuronal diversity in the cochlea is largely determined by ion channels. Among voltage-gated channels, hyperpolarization-activated cyclic nucleotide-gated (HCN) channels open with hyperpolarization and depolarize the cell until the resting membrane potential. The functions for hearing are not well elucidated and knowledge about localization is controversial. We created a detailed map of subcellular location and co-expression of all four HCN subunits across different mammalian species including CBA/J, C57Bl/6N, Ly5.1 mice, guinea pigs, cats, and human subjects. We correlated age-related hearing deterioration in CBA/J and C57Bl/6N with expression levels of HCN1, -2, and -4 in individual auditory neurons from the same cohort. Spatiotemporal expression during murine postnatal development exposed HCN2 and HCN4 involvement in a critical phase of hair cell innervation. The huge diversity of subunit composition, but lack of relevant heteromeric pairing along the perisomatic membrane and axon initial segments, highlighted an active role for auditory neurons. Neuron clusters were found to be the hot spots of HCN1, -2, and -4 immunostaining. HCN channels were also located in afferent and efferent fibers of the sensory epithelium. Age-related changes on HCN subtype expression were not uniform among mice and could not be directly correlated with audiometric data. The oldest mice groups revealed HCN channel up- or downregulation, depending on the mouse strain. The unexpected involvement of HCN channels in outer hair cell function where HCN3 overlaps prestin location emphasized the importance for auditory function. A better understanding may open up new possibilities to tune neuronal responses evoked through electrical stimulation by cochlear implants. Neuronal diversity in the cochlea is largely determined by ion channels. Among voltage‐gated channels, hyperpolarization‐activated cyclic nucleotide‐gated (HCN) channels open with hyperpolarization and depolarize the cell until the resting membrane potential. The functions for hearing are not well elucidated and knowledge about localization is controversial. We created a detailed map of subcellular location and co‐expression of all four HCN subunits across different mammalian species including CBA/J, C57Bl/6N, Ly5.1 mice, guinea pigs, cats, and human subjects. We correlated age‐related hearing deterioration in CBA/J and C57Bl/6N with expression levels of HCN1, −2, and −4 in individual auditory neurons from the same cohort. Spatiotemporal expression during murine postnatal development exposed HCN2 and HCN4 involvement in a critical phase of hair cell innervation. The huge diversity of subunit composition, but lack of relevant heteromeric pairing along the perisomatic membrane and axon initial segments, highlighted an active role for auditory neurons. Neuron clusters were found to be the hot spots of HCN1, −2, and −4 immunostaining. HCN channels were also located in afferent and efferent fibers of the sensory epithelium. Age‐related changes on HCN subtype expression were not uniform among mice and could not be directly correlated with audiometric data. The oldest mice groups revealed HCN channel up‐ or downregulation, depending on the mouse strain. The unexpected involvement of HCN channels in outer hair cell function where HCN3 overlaps prestin location emphasized the importance for auditory function. A better understanding may open up new possibilities to tune neuronal responses evoked through electrical stimulation by cochlear implants. |
| Author | Schrott‐Fischer, Anneliese Rask‐Andersen, Helge Dudas, Jozsef Liu, Wei Glueckert, Rudolf Pechriggl, Elisabeth Luque, Maria Brenner, Erich |
| AuthorAffiliation | 2 Department of Anatomy, Histology & Embryology Division of Clinical & Functional Anatomy Medical University of Innsbruck Innsbruck Austria 4 Tirol Kliniken University Clinics Innsbruck Innsbruck Austria 3 Department of Surgical Sciences, Head and Neck Surgery Section of Otolaryngology Uppsala University Hospital Uppsala Sweden 1 Department of Otorhinolaryngology Medical University of Innsbruck Innsbruck Austria |
| AuthorAffiliation_xml | – name: 4 Tirol Kliniken University Clinics Innsbruck Innsbruck Austria – name: 1 Department of Otorhinolaryngology Medical University of Innsbruck Innsbruck Austria – name: 2 Department of Anatomy, Histology & Embryology Division of Clinical & Functional Anatomy Medical University of Innsbruck Innsbruck Austria – name: 3 Department of Surgical Sciences, Head and Neck Surgery Section of Otolaryngology Uppsala University Hospital Uppsala Sweden |
| Author_xml | – sequence: 1 givenname: Maria surname: Luque fullname: Luque, Maria organization: Medical University of Innsbruck – sequence: 2 givenname: Anneliese orcidid: 0000-0002-4514-9867 surname: Schrott‐Fischer fullname: Schrott‐Fischer, Anneliese organization: Medical University of Innsbruck – sequence: 3 givenname: Jozsef surname: Dudas fullname: Dudas, Jozsef organization: Medical University of Innsbruck – sequence: 4 givenname: Elisabeth surname: Pechriggl fullname: Pechriggl, Elisabeth organization: Medical University of Innsbruck – sequence: 5 givenname: Erich orcidid: 0000-0001-6739-1198 surname: Brenner fullname: Brenner, Erich organization: Medical University of Innsbruck – sequence: 6 givenname: Helge surname: Rask‐Andersen fullname: Rask‐Andersen, Helge organization: Uppsala University Hospital – sequence: 7 givenname: Wei surname: Liu fullname: Liu, Wei organization: Uppsala University Hospital – sequence: 8 givenname: Rudolf orcidid: 0000-0002-2900-6866 surname: Glueckert fullname: Glueckert, Rudolf email: rudolf.glueckert@i-med.ac.at organization: University Clinics Innsbruck |
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| Snippet | Neuronal diversity in the cochlea is largely determined by ion channels. Among voltage‐gated channels, hyperpolarization‐activated cyclic nucleotide‐gated... Neuronal diversity in the cochlea is largely determined by ion channels. Among voltage-gated channels, hyperpolarization-activated cyclic nucleotide-gated... |
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| SubjectTerms | AB_2039906 AB_2302038 AB_2313584 AB_2313726 AB_2336419 AB_2336420 AB_2336790 AB_2340452 AB_2340477 AB_2340593 AB_2341028 AB_2617143 AB_2756625 AB_2756742 AB_90725 Age auditory development auditory neuron diversity Auditory system axon initial segment Cochlea Cochlear implants Depolarization Electrical stimuli Epithelium Fibers Guinea pigs Hair HCN channels Hearing Hyperpolarization Innervation Ion channels Ion channels (cyclic nucleotide-gated) Localization Mammals Membrane potential Membranes Neurons Nucleotides prestin RRID RRID:AB_2039906 RRID:AB_2302038 RRID:AB_2313584 RRID:AB_2313726 RRID:AB_2336419 RRID:AB_2336420 RRID:AB_2336790 RRID:AB_2340452 RRID:AB_2340477 RRID:AB_2340593 RRID:AB_2341028 RRID:AB_2617143 RRID:AB_2756625 RRID:AB_2756742 RRID:AB_90725 RRID:SCR_002865 RRID:SCR_013652 RRID:SCR_014823 SCR_002865 SCR_013652 SCR_014823 Sensory epithelium Sensory neurons Sensory stimulation sound coding spiral ganglion neurons Subunit structure voltage gated |
| Title | HCN channels in the mammalian cochlea: Expression pattern, subcellular location, and age‐dependent changes |
| URI | https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fjnr.24754 https://www.ncbi.nlm.nih.gov/pubmed/33181864 https://www.proquest.com/docview/2471172299 https://www.proquest.com/docview/2460761412 https://pubmed.ncbi.nlm.nih.gov/PMC7839784 https://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-438945 |
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