Glucose Starvation Inhibits Ferroptosis by Activating the LKB1/AMPK Signaling Pathway and Promotes the High Speed Linear Motility of Dairy Goat Sperm
In mammals, sperm acquire fertilization ability after capacitation in vitro or when in the female reproductive tract. The motility patterns of sperm undergo continuous changes from the moment of ejaculation until fertilization in the female reproductive tract. In vitro, hyperactivated motility can b...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2023-04-01
|
| Series: | Animals |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2076-2615/13/9/1442 |
| _version_ | 1797603116144656384 |
|---|---|
| author | Yu Li Guangzhi Zhang Fei Wen Ming Xian Songmao Guo Xing Zhang Xianzhou Feng Zhangtao Hu Jianhong Hu |
| author_facet | Yu Li Guangzhi Zhang Fei Wen Ming Xian Songmao Guo Xing Zhang Xianzhou Feng Zhangtao Hu Jianhong Hu |
| author_sort | Yu Li |
| collection | DOAJ |
| description | In mammals, sperm acquire fertilization ability after capacitation in vitro or when in the female reproductive tract. The motility patterns of sperm undergo continuous changes from the moment of ejaculation until fertilization in the female reproductive tract. In vitro, hyperactivated motility can be induced through high glucose mediums, while in vivo, it is induced by oviduct fluids. Conversely, sperm maintain linear motility in seminal plasma or uterine fluids that contain low glucose levels. In dairy goat sperm, energy metabolism associated with capacitation depends on the energy sources in vitro, seminal plasma, or the female reproductive tract, especially the glucose levels. However, there is little experimental knowledge that glucose levels affect sperm energy metabolism in dairy goats. To clarify these hypotheses, we incubated dairy goat spermatozoa with different concentrations of rotenone-glucose (ROT), carbonyl cyanide 4-(trifluoromethoxy) phenylhydrazone (FCCP), and tigecycline (TIG) in vitro. Sperm motility attributes, ATP content, pyruvate and lactate levels, mitochondrial permeability transition pore fluorescence intensity, mitochondrial membrane potential (MMP), and protein synthesis were analyzed. Sperm motility patterns changed from circular to linear under low glucose conditions compared with those in high glucose conditions and showed a significant improvement in progressive motility and straight line speed, whereas lactate and pyruvate levels and MMP decreased remarkably. Incubation of spermatozoa with ROT, FCCP, and TIG inhibited sperm mitochondrial activity, protein synthesis, oxidative phosphorylation, and ATP levels, thereby reducing sperm motility, including the progressive motility, straight line speed, and total motility. Simultaneously, incubation of spermatozoa with Compound C under low glucose conditions significantly decreased the ATP levels and MMP, as well as liver kinase B1 and AMPK protein expression. Under low glucose conditions, sperm mainly produce ATP through mitochondrial OXPHOS to achieve high speed linear movement, inhibit ferroptosis through the LKB1/AMPK signaling pathway, and further maintain energy metabolism homeostasis. |
| first_indexed | 2024-03-11T04:24:52Z |
| format | Article |
| id | doaj.art-1fa57df607d84533b83c49017d71e5b7 |
| institution | Directory Open Access Journal |
| issn | 2076-2615 |
| language | English |
| last_indexed | 2024-03-11T04:24:52Z |
| publishDate | 2023-04-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Animals |
| spelling | doaj.art-1fa57df607d84533b83c49017d71e5b72023-11-17T22:29:10ZengMDPI AGAnimals2076-26152023-04-01139144210.3390/ani13091442Glucose Starvation Inhibits Ferroptosis by Activating the LKB1/AMPK Signaling Pathway and Promotes the High Speed Linear Motility of Dairy Goat SpermYu Li0Guangzhi Zhang1Fei Wen2Ming Xian3Songmao Guo4Xing Zhang5Xianzhou Feng6Zhangtao Hu7Jianhong Hu8Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, ChinaIn mammals, sperm acquire fertilization ability after capacitation in vitro or when in the female reproductive tract. The motility patterns of sperm undergo continuous changes from the moment of ejaculation until fertilization in the female reproductive tract. In vitro, hyperactivated motility can be induced through high glucose mediums, while in vivo, it is induced by oviduct fluids. Conversely, sperm maintain linear motility in seminal plasma or uterine fluids that contain low glucose levels. In dairy goat sperm, energy metabolism associated with capacitation depends on the energy sources in vitro, seminal plasma, or the female reproductive tract, especially the glucose levels. However, there is little experimental knowledge that glucose levels affect sperm energy metabolism in dairy goats. To clarify these hypotheses, we incubated dairy goat spermatozoa with different concentrations of rotenone-glucose (ROT), carbonyl cyanide 4-(trifluoromethoxy) phenylhydrazone (FCCP), and tigecycline (TIG) in vitro. Sperm motility attributes, ATP content, pyruvate and lactate levels, mitochondrial permeability transition pore fluorescence intensity, mitochondrial membrane potential (MMP), and protein synthesis were analyzed. Sperm motility patterns changed from circular to linear under low glucose conditions compared with those in high glucose conditions and showed a significant improvement in progressive motility and straight line speed, whereas lactate and pyruvate levels and MMP decreased remarkably. Incubation of spermatozoa with ROT, FCCP, and TIG inhibited sperm mitochondrial activity, protein synthesis, oxidative phosphorylation, and ATP levels, thereby reducing sperm motility, including the progressive motility, straight line speed, and total motility. Simultaneously, incubation of spermatozoa with Compound C under low glucose conditions significantly decreased the ATP levels and MMP, as well as liver kinase B1 and AMPK protein expression. Under low glucose conditions, sperm mainly produce ATP through mitochondrial OXPHOS to achieve high speed linear movement, inhibit ferroptosis through the LKB1/AMPK signaling pathway, and further maintain energy metabolism homeostasis.https://www.mdpi.com/2076-2615/13/9/1442dairy goatspermglucosemitochondrial oxidative phosphorylationAMPKferroptosis |
| spellingShingle | Yu Li Guangzhi Zhang Fei Wen Ming Xian Songmao Guo Xing Zhang Xianzhou Feng Zhangtao Hu Jianhong Hu Glucose Starvation Inhibits Ferroptosis by Activating the LKB1/AMPK Signaling Pathway and Promotes the High Speed Linear Motility of Dairy Goat Sperm Animals dairy goat sperm glucose mitochondrial oxidative phosphorylation AMPK ferroptosis |
| title | Glucose Starvation Inhibits Ferroptosis by Activating the LKB1/AMPK Signaling Pathway and Promotes the High Speed Linear Motility of Dairy Goat Sperm |
| title_full | Glucose Starvation Inhibits Ferroptosis by Activating the LKB1/AMPK Signaling Pathway and Promotes the High Speed Linear Motility of Dairy Goat Sperm |
| title_fullStr | Glucose Starvation Inhibits Ferroptosis by Activating the LKB1/AMPK Signaling Pathway and Promotes the High Speed Linear Motility of Dairy Goat Sperm |
| title_full_unstemmed | Glucose Starvation Inhibits Ferroptosis by Activating the LKB1/AMPK Signaling Pathway and Promotes the High Speed Linear Motility of Dairy Goat Sperm |
| title_short | Glucose Starvation Inhibits Ferroptosis by Activating the LKB1/AMPK Signaling Pathway and Promotes the High Speed Linear Motility of Dairy Goat Sperm |
| title_sort | glucose starvation inhibits ferroptosis by activating the lkb1 ampk signaling pathway and promotes the high speed linear motility of dairy goat sperm |
| topic | dairy goat sperm glucose mitochondrial oxidative phosphorylation AMPK ferroptosis |
| url | https://www.mdpi.com/2076-2615/13/9/1442 |
| work_keys_str_mv | AT yuli glucosestarvationinhibitsferroptosisbyactivatingthelkb1ampksignalingpathwayandpromotesthehighspeedlinearmotilityofdairygoatsperm AT guangzhizhang glucosestarvationinhibitsferroptosisbyactivatingthelkb1ampksignalingpathwayandpromotesthehighspeedlinearmotilityofdairygoatsperm AT feiwen glucosestarvationinhibitsferroptosisbyactivatingthelkb1ampksignalingpathwayandpromotesthehighspeedlinearmotilityofdairygoatsperm AT mingxian glucosestarvationinhibitsferroptosisbyactivatingthelkb1ampksignalingpathwayandpromotesthehighspeedlinearmotilityofdairygoatsperm AT songmaoguo glucosestarvationinhibitsferroptosisbyactivatingthelkb1ampksignalingpathwayandpromotesthehighspeedlinearmotilityofdairygoatsperm AT xingzhang glucosestarvationinhibitsferroptosisbyactivatingthelkb1ampksignalingpathwayandpromotesthehighspeedlinearmotilityofdairygoatsperm AT xianzhoufeng glucosestarvationinhibitsferroptosisbyactivatingthelkb1ampksignalingpathwayandpromotesthehighspeedlinearmotilityofdairygoatsperm AT zhangtaohu glucosestarvationinhibitsferroptosisbyactivatingthelkb1ampksignalingpathwayandpromotesthehighspeedlinearmotilityofdairygoatsperm AT jianhonghu glucosestarvationinhibitsferroptosisbyactivatingthelkb1ampksignalingpathwayandpromotesthehighspeedlinearmotilityofdairygoatsperm |