Sleep deprivation induces delayed regeneration of olfactory sensory neurons following injury
The circadian system, which is essential for the alignment of sleep/wake cycles, modulates adult neurogenesis. The olfactory epithelium (OE) has the ability to generate new neurons throughout life. Loss of olfactory sensory neurons (OSNs) as a result of injury to the OE triggers the generation of ne...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-12-01
|
| Series: | Frontiers in Neuroscience |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2022.1029279/full |
| _version_ | 1798014913037205504 |
|---|---|
| author | Bing Han Shu Kikuta Teru Kamogashira Kenji Kondo Tatsuya Yamasoba |
| author_facet | Bing Han Shu Kikuta Teru Kamogashira Kenji Kondo Tatsuya Yamasoba |
| author_sort | Bing Han |
| collection | DOAJ |
| description | The circadian system, which is essential for the alignment of sleep/wake cycles, modulates adult neurogenesis. The olfactory epithelium (OE) has the ability to generate new neurons throughout life. Loss of olfactory sensory neurons (OSNs) as a result of injury to the OE triggers the generation of new OSNs, which are incorporated into olfactory circuits to restore olfactory sensory perception. This regenerative potential means that it is likely that the OE is substantially affected by sleep deprivation (SD), although how this may occur remains unclear. The aim of this study is to address how SD affects the process of OSN regeneration following OE injury. Mice were subjected to SD for 2 weeks, which induced changes in circadian activity. This condition resulted in decreased activity during the night-time and increased activity during the daytime, and induced no histological changes in the OE. However, when subjected to SD during the regeneration process after OE injury, a significant decrease in the number of mature OSNs in the dorsomedial area of the OE, which is the only area containing neurons expressing NQO1 (quinone dehydrogenase 1), was observed compared to the NQO1-negative OE. Furthermore, a significant decrease in proliferating basal cells was observed in the NQO1-positive OE compared to the NQO1-negative OE, but no increase in apoptotic OSNs was observed. These results indicate that SD accompanied by disturbed circadian activity could induce structurally negative effects on OSN regeneration, preferentially in the dorsomedial area of the OE, and that this area-specific regeneration delay might involve the biological activity of NQO1. |
| first_indexed | 2024-04-11T15:26:01Z |
| format | Article |
| id | doaj.art-9ad4256871bc47b0b993223dd9094a15 |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-04-11T15:26:01Z |
| publishDate | 2022-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj.art-9ad4256871bc47b0b993223dd9094a152022-12-22T04:16:15ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2022-12-011610.3389/fnins.2022.10292791029279Sleep deprivation induces delayed regeneration of olfactory sensory neurons following injuryBing HanShu KikutaTeru KamogashiraKenji KondoTatsuya YamasobaThe circadian system, which is essential for the alignment of sleep/wake cycles, modulates adult neurogenesis. The olfactory epithelium (OE) has the ability to generate new neurons throughout life. Loss of olfactory sensory neurons (OSNs) as a result of injury to the OE triggers the generation of new OSNs, which are incorporated into olfactory circuits to restore olfactory sensory perception. This regenerative potential means that it is likely that the OE is substantially affected by sleep deprivation (SD), although how this may occur remains unclear. The aim of this study is to address how SD affects the process of OSN regeneration following OE injury. Mice were subjected to SD for 2 weeks, which induced changes in circadian activity. This condition resulted in decreased activity during the night-time and increased activity during the daytime, and induced no histological changes in the OE. However, when subjected to SD during the regeneration process after OE injury, a significant decrease in the number of mature OSNs in the dorsomedial area of the OE, which is the only area containing neurons expressing NQO1 (quinone dehydrogenase 1), was observed compared to the NQO1-negative OE. Furthermore, a significant decrease in proliferating basal cells was observed in the NQO1-positive OE compared to the NQO1-negative OE, but no increase in apoptotic OSNs was observed. These results indicate that SD accompanied by disturbed circadian activity could induce structurally negative effects on OSN regeneration, preferentially in the dorsomedial area of the OE, and that this area-specific regeneration delay might involve the biological activity of NQO1.https://www.frontiersin.org/articles/10.3389/fnins.2022.1029279/fullolfactory sensory neuronolfactory dysfunctionquinone dehydrogenase 1sleep deprivationcircadian activity |
| spellingShingle | Bing Han Shu Kikuta Teru Kamogashira Kenji Kondo Tatsuya Yamasoba Sleep deprivation induces delayed regeneration of olfactory sensory neurons following injury Frontiers in Neuroscience olfactory sensory neuron olfactory dysfunction quinone dehydrogenase 1 sleep deprivation circadian activity |
| title | Sleep deprivation induces delayed regeneration of olfactory sensory neurons following injury |
| title_full | Sleep deprivation induces delayed regeneration of olfactory sensory neurons following injury |
| title_fullStr | Sleep deprivation induces delayed regeneration of olfactory sensory neurons following injury |
| title_full_unstemmed | Sleep deprivation induces delayed regeneration of olfactory sensory neurons following injury |
| title_short | Sleep deprivation induces delayed regeneration of olfactory sensory neurons following injury |
| title_sort | sleep deprivation induces delayed regeneration of olfactory sensory neurons following injury |
| topic | olfactory sensory neuron olfactory dysfunction quinone dehydrogenase 1 sleep deprivation circadian activity |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2022.1029279/full |
| work_keys_str_mv | AT binghan sleepdeprivationinducesdelayedregenerationofolfactorysensoryneuronsfollowinginjury AT shukikuta sleepdeprivationinducesdelayedregenerationofolfactorysensoryneuronsfollowinginjury AT terukamogashira sleepdeprivationinducesdelayedregenerationofolfactorysensoryneuronsfollowinginjury AT kenjikondo sleepdeprivationinducesdelayedregenerationofolfactorysensoryneuronsfollowinginjury AT tatsuyayamasoba sleepdeprivationinducesdelayedregenerationofolfactorysensoryneuronsfollowinginjury |