Neuronal Cytoglobin in the Auditory Brainstem of Rat and Mouse: Distribution, Cochlear Projection, and Nitric Oxide Production
Cytoglobin (Cygb), a hemoprotein of the globin family, is expressed in the supportive tissue cells of the fibroblast lineage and in distinct neuronal cell populations. The expression pattern and regulatory parameters of fibroblasts and related cells were studied in organs such as the kidney and live...
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| Format: | Article |
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MDPI AG
2023-01-01
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| Series: | Brain Sciences |
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| Online Access: | https://www.mdpi.com/2076-3425/13/1/107 |
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| author | Stefan Reuss Daniel Balmaceda Mirra Elgurt Randolf Riemann |
| author_facet | Stefan Reuss Daniel Balmaceda Mirra Elgurt Randolf Riemann |
| author_sort | Stefan Reuss |
| collection | DOAJ |
| description | Cytoglobin (Cygb), a hemoprotein of the globin family, is expressed in the supportive tissue cells of the fibroblast lineage and in distinct neuronal cell populations. The expression pattern and regulatory parameters of fibroblasts and related cells were studied in organs such as the kidney and liver in a variety of animal models. In contrast, knowledge about cytoglobin-expressing neurons is sparse. Only a few papers described the distribution in the brain as ubiquitous with a restricted number of neurons in focal regions. Although there is evidence for cytoglobin involvement in neuronal hypoxia tolerance, its presence in the auditory system was not studied despite high metabolism rates and oxygen demands of the cochlea and related brainstem centers. In a continuation of a previous study demonstrating Cygb-neurons in, inter alia, auditory regions of the mouse brain, we concentrated on the superior olivary complex (SOC) in the present study. We sought to investigate the distribution, projection pattern and neurochemistry of Cygb-neurons in the SOC. We conducted immunohistochemistry using a Cygb antibody and found that this brainstem region, functionally competent for bilateral hearing and providing cochlear hair cell innervation, contains a considerable number of Cygb-expressing neurons (averaging 2067 ± 211 making up 10 ±1% percent of total neuron number) in rats, and 514 ± 138 (6 ± 1%) in mice. They were observed in all regions of the SOC. Retrograde neuronal tract tracing with Fluorogold injected into the cochlea demonstrated that 1243 ± 100 (6 ± 1% of total neuron number in rat SOC)) were olivocochlear neurons. Approximately 56% of total Cygb neurons were retrogradely labelled, while the majority of olivocochlear neurons of both lateral and medial systems were Cygb-immunoreactive. We also conducted double immunofluorescence staining for Cygb and neuronal nitric oxide synthase (nNOS), the enzyme responsible for nitric oxide production, and observed that cytoglobin in the SOC frequently co-localized with nNOS. Our findings suggest that cytoglobin plays an important physiologic role in the oxygen homeostasis of the peripheral and central auditory nervous system. Further studies, also including transgenic animal models, are required to shed more light on the function(s) of Cygb in neurons, in particular of the auditory system. |
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| format | Article |
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| institution | Directory Open Access Journal |
| issn | 2076-3425 |
| language | English |
| last_indexed | 2024-03-09T13:22:33Z |
| publishDate | 2023-01-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Brain Sciences |
| spelling | doaj.art-9a955a99c8684cfea8d0bad4f2006f592023-11-30T21:27:45ZengMDPI AGBrain Sciences2076-34252023-01-0113110710.3390/brainsci13010107Neuronal Cytoglobin in the Auditory Brainstem of Rat and Mouse: Distribution, Cochlear Projection, and Nitric Oxide ProductionStefan Reuss0Daniel Balmaceda1Mirra Elgurt2Randolf Riemann3Department of Nuclear Medicine, University Medical Center, Johannes Gutenberg-University, 55101 Mainz, GermanyDepartment of Anatomy and Cell Biology, University Medical Center, Johannes Gutenberg-University, 55099 Mainz, GermanyDepartment of Anatomy and Cell Biology, University Medical Center, Johannes Gutenberg-University, 55099 Mainz, GermanyDepartment of Otorhinolaryngology, Elbe-Kliniken, 21682 Stade, GermanyCytoglobin (Cygb), a hemoprotein of the globin family, is expressed in the supportive tissue cells of the fibroblast lineage and in distinct neuronal cell populations. The expression pattern and regulatory parameters of fibroblasts and related cells were studied in organs such as the kidney and liver in a variety of animal models. In contrast, knowledge about cytoglobin-expressing neurons is sparse. Only a few papers described the distribution in the brain as ubiquitous with a restricted number of neurons in focal regions. Although there is evidence for cytoglobin involvement in neuronal hypoxia tolerance, its presence in the auditory system was not studied despite high metabolism rates and oxygen demands of the cochlea and related brainstem centers. In a continuation of a previous study demonstrating Cygb-neurons in, inter alia, auditory regions of the mouse brain, we concentrated on the superior olivary complex (SOC) in the present study. We sought to investigate the distribution, projection pattern and neurochemistry of Cygb-neurons in the SOC. We conducted immunohistochemistry using a Cygb antibody and found that this brainstem region, functionally competent for bilateral hearing and providing cochlear hair cell innervation, contains a considerable number of Cygb-expressing neurons (averaging 2067 ± 211 making up 10 ±1% percent of total neuron number) in rats, and 514 ± 138 (6 ± 1%) in mice. They were observed in all regions of the SOC. Retrograde neuronal tract tracing with Fluorogold injected into the cochlea demonstrated that 1243 ± 100 (6 ± 1% of total neuron number in rat SOC)) were olivocochlear neurons. Approximately 56% of total Cygb neurons were retrogradely labelled, while the majority of olivocochlear neurons of both lateral and medial systems were Cygb-immunoreactive. We also conducted double immunofluorescence staining for Cygb and neuronal nitric oxide synthase (nNOS), the enzyme responsible for nitric oxide production, and observed that cytoglobin in the SOC frequently co-localized with nNOS. Our findings suggest that cytoglobin plays an important physiologic role in the oxygen homeostasis of the peripheral and central auditory nervous system. Further studies, also including transgenic animal models, are required to shed more light on the function(s) of Cygb in neurons, in particular of the auditory system.https://www.mdpi.com/2076-3425/13/1/107cytoglobinmicehearingauditoryratimmunohistochemistry |
| spellingShingle | Stefan Reuss Daniel Balmaceda Mirra Elgurt Randolf Riemann Neuronal Cytoglobin in the Auditory Brainstem of Rat and Mouse: Distribution, Cochlear Projection, and Nitric Oxide Production Brain Sciences cytoglobin mice hearing auditory rat immunohistochemistry |
| title | Neuronal Cytoglobin in the Auditory Brainstem of Rat and Mouse: Distribution, Cochlear Projection, and Nitric Oxide Production |
| title_full | Neuronal Cytoglobin in the Auditory Brainstem of Rat and Mouse: Distribution, Cochlear Projection, and Nitric Oxide Production |
| title_fullStr | Neuronal Cytoglobin in the Auditory Brainstem of Rat and Mouse: Distribution, Cochlear Projection, and Nitric Oxide Production |
| title_full_unstemmed | Neuronal Cytoglobin in the Auditory Brainstem of Rat and Mouse: Distribution, Cochlear Projection, and Nitric Oxide Production |
| title_short | Neuronal Cytoglobin in the Auditory Brainstem of Rat and Mouse: Distribution, Cochlear Projection, and Nitric Oxide Production |
| title_sort | neuronal cytoglobin in the auditory brainstem of rat and mouse distribution cochlear projection and nitric oxide production |
| topic | cytoglobin mice hearing auditory rat immunohistochemistry |
| url | https://www.mdpi.com/2076-3425/13/1/107 |
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