The relationship between gut microbiota and inflammatory response, learning and memory in mice by sleep deprivation
ObjectiveSleep deprivation has developed into a common phenomenon, which can lead to inflammatory responses and cognitive impairment, but the underlying mechanism is ambiguous. Emerging evidence shows that gut microbiota plays a crucial role in theoccurrence and development of inflammatory and psych...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2023-05-01
|
| Series: | Frontiers in Cellular and Infection Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fcimb.2023.1159771/full |
| _version_ | 1797821531333591040 |
|---|---|
| author | Mengjie Zhang Mengjie Zhang Mengying Zhang Mengying Zhang Guangning Kou Yan Li Yan Li |
| author_facet | Mengjie Zhang Mengjie Zhang Mengying Zhang Mengying Zhang Guangning Kou Yan Li Yan Li |
| author_sort | Mengjie Zhang |
| collection | DOAJ |
| description | ObjectiveSleep deprivation has developed into a common phenomenon, which can lead to inflammatory responses and cognitive impairment, but the underlying mechanism is ambiguous. Emerging evidence shows that gut microbiota plays a crucial role in theoccurrence and development of inflammatory and psychiatric diseases, possibly through neuroinflammation and the brain-gut axis. The current study investigated the influence of sleep deprivation on gut microbiota composition, pro-inflammatory cytokines, learning and memory in mice. Further, it explored whether changes in gut microbiota increase pro-inflammatory cytokine and induce learning and memory impairment.MethodsHealthy 8-week-old male C57BL/6J mice were randomly divided into the regular control group (RC), environmental control group (EC), and sleep deprivation group (SD). The sleep deprivation model was established by the Modified Multiple Platform Method. The experimental mice were subjected to sleep deprivation for 6h/d (8:00 am∼14:00 pm) in a sleep deprivation chamber, and the duration of sleep deprivation was 8 weeks. Morris water maze test to assess learning and memory in mice. Enzyme-Linked Immunosorbent Assay determined the concentrations of inflammatory cytokines. The changes in gut microbiota in mice were analyzed by 16S rRNA sequencing.ResultsWe found that SD mice had elevated latency of exploration to reach the hidden platform (p>0.05) and significantly decreased traversing times, swimming distance, and swimming time in the target zone when the hidden platform was removed (p<0.05). Sleep deprivation caused dysregulated expression in serum IL-1β, IL-6, and TNF-α in mice, and the difference was significant (all p<0.001). Tannerellaceae, Rhodospirillales, Alistipes, and Parabacteroides were significantly increased in SD mice. Correlation analysis showed IL-1β was positively correlated with the abundance of Muribaculaceae (r=0.497, p<0.05) and negatively correlated with the abundance of Lachnospiraceae (r=-0.583, p<0.05). The TNF-α was positively correlated with the abundances of Erysipelotrichaceae, Burkholderiaceae, and Tannerellaceae (r=0.492, r=0.646, r=0.726, all p<0.05).ConclusionSleep deprivation can increase pro-inflammatory cytokine responses and learning and memory impairment in mice and may be caused by the disorder of the microbiota. These findings of this study may open avenues for potential interventions that can relieve the detrimental consequences of sleep loss. |
| first_indexed | 2024-03-13T09:54:07Z |
| format | Article |
| id | doaj.art-f056f5b98b5544b68385eeb14baf1ba6 |
| institution | Directory Open Access Journal |
| issn | 2235-2988 |
| language | English |
| last_indexed | 2024-03-13T09:54:07Z |
| publishDate | 2023-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular and Infection Microbiology |
| spelling | doaj.art-f056f5b98b5544b68385eeb14baf1ba62023-05-24T05:14:42ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882023-05-011310.3389/fcimb.2023.11597711159771The relationship between gut microbiota and inflammatory response, learning and memory in mice by sleep deprivationMengjie Zhang0Mengjie Zhang1Mengying Zhang2Mengying Zhang3Guangning Kou4Yan Li5Yan Li6School of Physical Education and Sport Science, Fujian Normal University, Fuzhou, ChinaZhengzhou University, Zhengzhou, ChinaZhengzhou University, Zhengzhou, ChinaSynergetic Innovation Center of Kinesis and Health, School of Physical Education (Main Campus), Zhengzhou University, Zhengzhou, ChinaCentre of Sport Nutrition and Health, School of Physical Education, Zhengzhou University, Zhengzhou, ChinaZhengzhou University, Zhengzhou, ChinaSynergetic Innovation Center of Kinesis and Health, School of Physical Education (Main Campus), Zhengzhou University, Zhengzhou, ChinaObjectiveSleep deprivation has developed into a common phenomenon, which can lead to inflammatory responses and cognitive impairment, but the underlying mechanism is ambiguous. Emerging evidence shows that gut microbiota plays a crucial role in theoccurrence and development of inflammatory and psychiatric diseases, possibly through neuroinflammation and the brain-gut axis. The current study investigated the influence of sleep deprivation on gut microbiota composition, pro-inflammatory cytokines, learning and memory in mice. Further, it explored whether changes in gut microbiota increase pro-inflammatory cytokine and induce learning and memory impairment.MethodsHealthy 8-week-old male C57BL/6J mice were randomly divided into the regular control group (RC), environmental control group (EC), and sleep deprivation group (SD). The sleep deprivation model was established by the Modified Multiple Platform Method. The experimental mice were subjected to sleep deprivation for 6h/d (8:00 am∼14:00 pm) in a sleep deprivation chamber, and the duration of sleep deprivation was 8 weeks. Morris water maze test to assess learning and memory in mice. Enzyme-Linked Immunosorbent Assay determined the concentrations of inflammatory cytokines. The changes in gut microbiota in mice were analyzed by 16S rRNA sequencing.ResultsWe found that SD mice had elevated latency of exploration to reach the hidden platform (p>0.05) and significantly decreased traversing times, swimming distance, and swimming time in the target zone when the hidden platform was removed (p<0.05). Sleep deprivation caused dysregulated expression in serum IL-1β, IL-6, and TNF-α in mice, and the difference was significant (all p<0.001). Tannerellaceae, Rhodospirillales, Alistipes, and Parabacteroides were significantly increased in SD mice. Correlation analysis showed IL-1β was positively correlated with the abundance of Muribaculaceae (r=0.497, p<0.05) and negatively correlated with the abundance of Lachnospiraceae (r=-0.583, p<0.05). The TNF-α was positively correlated with the abundances of Erysipelotrichaceae, Burkholderiaceae, and Tannerellaceae (r=0.492, r=0.646, r=0.726, all p<0.05).ConclusionSleep deprivation can increase pro-inflammatory cytokine responses and learning and memory impairment in mice and may be caused by the disorder of the microbiota. These findings of this study may open avenues for potential interventions that can relieve the detrimental consequences of sleep loss.https://www.frontiersin.org/articles/10.3389/fcimb.2023.1159771/fullsleep deprivationgut microbiotainflammationlearning and memorycognition |
| spellingShingle | Mengjie Zhang Mengjie Zhang Mengying Zhang Mengying Zhang Guangning Kou Yan Li Yan Li The relationship between gut microbiota and inflammatory response, learning and memory in mice by sleep deprivation Frontiers in Cellular and Infection Microbiology sleep deprivation gut microbiota inflammation learning and memory cognition |
| title | The relationship between gut microbiota and inflammatory response, learning and memory in mice by sleep deprivation |
| title_full | The relationship between gut microbiota and inflammatory response, learning and memory in mice by sleep deprivation |
| title_fullStr | The relationship between gut microbiota and inflammatory response, learning and memory in mice by sleep deprivation |
| title_full_unstemmed | The relationship between gut microbiota and inflammatory response, learning and memory in mice by sleep deprivation |
| title_short | The relationship between gut microbiota and inflammatory response, learning and memory in mice by sleep deprivation |
| title_sort | relationship between gut microbiota and inflammatory response learning and memory in mice by sleep deprivation |
| topic | sleep deprivation gut microbiota inflammation learning and memory cognition |
| url | https://www.frontiersin.org/articles/10.3389/fcimb.2023.1159771/full |
| work_keys_str_mv | AT mengjiezhang therelationshipbetweengutmicrobiotaandinflammatoryresponselearningandmemoryinmicebysleepdeprivation AT mengjiezhang therelationshipbetweengutmicrobiotaandinflammatoryresponselearningandmemoryinmicebysleepdeprivation AT mengyingzhang therelationshipbetweengutmicrobiotaandinflammatoryresponselearningandmemoryinmicebysleepdeprivation AT mengyingzhang therelationshipbetweengutmicrobiotaandinflammatoryresponselearningandmemoryinmicebysleepdeprivation AT guangningkou therelationshipbetweengutmicrobiotaandinflammatoryresponselearningandmemoryinmicebysleepdeprivation AT yanli therelationshipbetweengutmicrobiotaandinflammatoryresponselearningandmemoryinmicebysleepdeprivation AT yanli therelationshipbetweengutmicrobiotaandinflammatoryresponselearningandmemoryinmicebysleepdeprivation AT mengjiezhang relationshipbetweengutmicrobiotaandinflammatoryresponselearningandmemoryinmicebysleepdeprivation AT mengjiezhang relationshipbetweengutmicrobiotaandinflammatoryresponselearningandmemoryinmicebysleepdeprivation AT mengyingzhang relationshipbetweengutmicrobiotaandinflammatoryresponselearningandmemoryinmicebysleepdeprivation AT mengyingzhang relationshipbetweengutmicrobiotaandinflammatoryresponselearningandmemoryinmicebysleepdeprivation AT guangningkou relationshipbetweengutmicrobiotaandinflammatoryresponselearningandmemoryinmicebysleepdeprivation AT yanli relationshipbetweengutmicrobiotaandinflammatoryresponselearningandmemoryinmicebysleepdeprivation AT yanli relationshipbetweengutmicrobiotaandinflammatoryresponselearningandmemoryinmicebysleepdeprivation |