Mouse sperm energy restriction and recovery (SER) revealed novel metabolic pathways
- Autores
- Romarowski, Ana; Fejzo, Jasna; Nayyab, Saman; Martín Hidalgo, David; Gervasi, Maria Gracia; Balbach, Melanie; Violante, Sara; Salicione, Ana M.; Cross, Justin; Levin, Lonny R.; Buck, Jochen; Visconti, Pablo E.
- Año de publicación
- 2023
- Idioma
- inglés
- Tipo de recurso
- artículo
- Estado
- versión publicada
- Descripción
- Mammalian sperm must undergo capacitation to become fertilization-competent. While working on mice, we recently developed a new methodology for treating sperm in vitro, which results in higher rates of fertilization and embryo development after in vitro fertilization. Sperm incubated in media devoid of nutrients lose motility, although they remain viable. Upon re-adding energy substrates, sperm resume motility and become capacitated with improved functionality. Here, we explore how sperm energy restriction and recovery (SER) treatment affects sperm metabolism and capacitation-associated signaling. Using extracellular flux analysis and metabolite profiling and tracing via nuclear magnetic resonance (NMR) and mass spectrometry (MS), we found that the levels of many metabolites were altered during the starvation phase of SER. Of particular interest, two metabolites, AMP and L-carnitine, were significantly increased in energy-restricted sperm. Upon re-addition of glucose and initiation of capacitation, most metabolite levels recovered and closely mimic the levels observed in capacitating sperm that have not undergone starvation. In both control and SER-treated sperm, incubation under capacitating conditions upregulated glycolysis and oxidative phosphorylation. However, ATP levels were diminished, presumably reflecting the increased energy consumption during capacitation. Flux data following the fate of 13C glucose indicate that, similar to other cells with high glucose consumption rates, pyruvate is converted into 13C-lactate and, with lower efficiency, into 13C-acetate, which are then released into the incubation media. Furthermore, our metabolic flux data show that exogenously supplied glucose is converted into citrate, providing evidence that in sperm cells, as in somatic cells, glycolytic products can be converted into Krebs cycle metabolites.
Fil: Romarowski, Ana. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Biología y Medicina Experimental. Fundación de Instituto de Biología y Medicina Experimental. Instituto de Biología y Medicina Experimental; Argentina. University of Massachussets; Estados Unidos
Fil: Fejzo, Jasna. University of Massachussets; Estados Unidos
Fil: Nayyab, Saman. University of Massachussets; Estados Unidos
Fil: Martín Hidalgo, David. Hospital San Pedro de Alcántara; España
Fil: Gervasi, Maria Gracia. University of Massachussets; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Balbach, Melanie. No especifíca;
Fil: Violante, Sara. No especifíca;
Fil: Salicione, Ana M.. University of Massachussets; Estados Unidos
Fil: Cross, Justin. No especifíca;
Fil: Levin, Lonny R.. No especifíca;
Fil: Buck, Jochen. No especifíca;
Fil: Visconti, Pablo E.. University of Massachussets; Estados Unidos - Materia
-
SPERM
ASSISTED REPRODUCTIVE TECHNOLOGIES
METABOLISM
AMP
ATP
CITRATE
L-CARNITINE - Nivel de accesibilidad
- acceso abierto
- Condiciones de uso
- https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
- Repositorio
.jpg)
- Institución
- Consejo Nacional de Investigaciones Científicas y Técnicas
- OAI Identificador
- oai:ri.conicet.gov.ar:11336/244026
Ver los metadatos del registro completo
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Mouse sperm energy restriction and recovery (SER) revealed novel metabolic pathwaysRomarowski, AnaFejzo, JasnaNayyab, SamanMartín Hidalgo, DavidGervasi, Maria GraciaBalbach, MelanieViolante, SaraSalicione, Ana M.Cross, JustinLevin, Lonny R.Buck, JochenVisconti, Pablo E.SPERMASSISTED REPRODUCTIVE TECHNOLOGIESMETABOLISMAMPATPCITRATEL-CARNITINEhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Mammalian sperm must undergo capacitation to become fertilization-competent. While working on mice, we recently developed a new methodology for treating sperm in vitro, which results in higher rates of fertilization and embryo development after in vitro fertilization. Sperm incubated in media devoid of nutrients lose motility, although they remain viable. Upon re-adding energy substrates, sperm resume motility and become capacitated with improved functionality. Here, we explore how sperm energy restriction and recovery (SER) treatment affects sperm metabolism and capacitation-associated signaling. Using extracellular flux analysis and metabolite profiling and tracing via nuclear magnetic resonance (NMR) and mass spectrometry (MS), we found that the levels of many metabolites were altered during the starvation phase of SER. Of particular interest, two metabolites, AMP and L-carnitine, were significantly increased in energy-restricted sperm. Upon re-addition of glucose and initiation of capacitation, most metabolite levels recovered and closely mimic the levels observed in capacitating sperm that have not undergone starvation. In both control and SER-treated sperm, incubation under capacitating conditions upregulated glycolysis and oxidative phosphorylation. However, ATP levels were diminished, presumably reflecting the increased energy consumption during capacitation. Flux data following the fate of 13C glucose indicate that, similar to other cells with high glucose consumption rates, pyruvate is converted into 13C-lactate and, with lower efficiency, into 13C-acetate, which are then released into the incubation media. Furthermore, our metabolic flux data show that exogenously supplied glucose is converted into citrate, providing evidence that in sperm cells, as in somatic cells, glycolytic products can be converted into Krebs cycle metabolites.Fil: Romarowski, Ana. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Biología y Medicina Experimental. Fundación de Instituto de Biología y Medicina Experimental. Instituto de Biología y Medicina Experimental; Argentina. University of Massachussets; Estados UnidosFil: Fejzo, Jasna. University of Massachussets; Estados UnidosFil: Nayyab, Saman. University of Massachussets; Estados UnidosFil: Martín Hidalgo, David. Hospital San Pedro de Alcántara; EspañaFil: Gervasi, Maria Gracia. University of Massachussets; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Balbach, Melanie. No especifíca;Fil: Violante, Sara. No especifíca;Fil: Salicione, Ana M.. University of Massachussets; Estados UnidosFil: Cross, Justin. No especifíca;Fil: Levin, Lonny R.. No especifíca;Fil: Buck, Jochen. No especifíca;Fil: Visconti, Pablo E.. University of Massachussets; Estados UnidosFrontiers Media2023-08info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/244026Romarowski, Ana; Fejzo, Jasna; Nayyab, Saman; Martín Hidalgo, David; Gervasi, Maria Gracia; et al.; Mouse sperm energy restriction and recovery (SER) revealed novel metabolic pathways; Frontiers Media; Frontiers in Cell and Developmental Biology; 11; 8-2023; 1-182296-634XCONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/journals/cell-and-developmental-biology/articles/10.3389/fcell.2023.1234221/fullinfo:eu-repo/semantics/altIdentifier/doi/10.3389/fcell.2023.1234221info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-10-22T11:04:55Zoai:ri.conicet.gov.ar:11336/244026instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-10-22 11:04:56.157CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse |
| dc.title.none.fl_str_mv |
Mouse sperm energy restriction and recovery (SER) revealed novel metabolic pathways |
| title |
Mouse sperm energy restriction and recovery (SER) revealed novel metabolic pathways |
| spellingShingle |
Mouse sperm energy restriction and recovery (SER) revealed novel metabolic pathways Romarowski, Ana SPERM ASSISTED REPRODUCTIVE TECHNOLOGIES METABOLISM AMP ATP CITRATE L-CARNITINE |
| title_short |
Mouse sperm energy restriction and recovery (SER) revealed novel metabolic pathways |
| title_full |
Mouse sperm energy restriction and recovery (SER) revealed novel metabolic pathways |
| title_fullStr |
Mouse sperm energy restriction and recovery (SER) revealed novel metabolic pathways |
| title_full_unstemmed |
Mouse sperm energy restriction and recovery (SER) revealed novel metabolic pathways |
| title_sort |
Mouse sperm energy restriction and recovery (SER) revealed novel metabolic pathways |
| dc.creator.none.fl_str_mv |
Romarowski, Ana Fejzo, Jasna Nayyab, Saman Martín Hidalgo, David Gervasi, Maria Gracia Balbach, Melanie Violante, Sara Salicione, Ana M. Cross, Justin Levin, Lonny R. Buck, Jochen Visconti, Pablo E. |
| author |
Romarowski, Ana |
| author_facet |
Romarowski, Ana Fejzo, Jasna Nayyab, Saman Martín Hidalgo, David Gervasi, Maria Gracia Balbach, Melanie Violante, Sara Salicione, Ana M. Cross, Justin Levin, Lonny R. Buck, Jochen Visconti, Pablo E. |
| author_role |
author |
| author2 |
Fejzo, Jasna Nayyab, Saman Martín Hidalgo, David Gervasi, Maria Gracia Balbach, Melanie Violante, Sara Salicione, Ana M. Cross, Justin Levin, Lonny R. Buck, Jochen Visconti, Pablo E. |
| author2_role |
author author author author author author author author author author author |
| dc.subject.none.fl_str_mv |
SPERM ASSISTED REPRODUCTIVE TECHNOLOGIES METABOLISM AMP ATP CITRATE L-CARNITINE |
| topic |
SPERM ASSISTED REPRODUCTIVE TECHNOLOGIES METABOLISM AMP ATP CITRATE L-CARNITINE |
| purl_subject.fl_str_mv |
https://purl.org/becyt/ford/1.6 https://purl.org/becyt/ford/1 |
| dc.description.none.fl_txt_mv |
Mammalian sperm must undergo capacitation to become fertilization-competent. While working on mice, we recently developed a new methodology for treating sperm in vitro, which results in higher rates of fertilization and embryo development after in vitro fertilization. Sperm incubated in media devoid of nutrients lose motility, although they remain viable. Upon re-adding energy substrates, sperm resume motility and become capacitated with improved functionality. Here, we explore how sperm energy restriction and recovery (SER) treatment affects sperm metabolism and capacitation-associated signaling. Using extracellular flux analysis and metabolite profiling and tracing via nuclear magnetic resonance (NMR) and mass spectrometry (MS), we found that the levels of many metabolites were altered during the starvation phase of SER. Of particular interest, two metabolites, AMP and L-carnitine, were significantly increased in energy-restricted sperm. Upon re-addition of glucose and initiation of capacitation, most metabolite levels recovered and closely mimic the levels observed in capacitating sperm that have not undergone starvation. In both control and SER-treated sperm, incubation under capacitating conditions upregulated glycolysis and oxidative phosphorylation. However, ATP levels were diminished, presumably reflecting the increased energy consumption during capacitation. Flux data following the fate of 13C glucose indicate that, similar to other cells with high glucose consumption rates, pyruvate is converted into 13C-lactate and, with lower efficiency, into 13C-acetate, which are then released into the incubation media. Furthermore, our metabolic flux data show that exogenously supplied glucose is converted into citrate, providing evidence that in sperm cells, as in somatic cells, glycolytic products can be converted into Krebs cycle metabolites. Fil: Romarowski, Ana. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Biología y Medicina Experimental. Fundación de Instituto de Biología y Medicina Experimental. Instituto de Biología y Medicina Experimental; Argentina. University of Massachussets; Estados Unidos Fil: Fejzo, Jasna. University of Massachussets; Estados Unidos Fil: Nayyab, Saman. University of Massachussets; Estados Unidos Fil: Martín Hidalgo, David. Hospital San Pedro de Alcántara; España Fil: Gervasi, Maria Gracia. University of Massachussets; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina Fil: Balbach, Melanie. No especifíca; Fil: Violante, Sara. No especifíca; Fil: Salicione, Ana M.. University of Massachussets; Estados Unidos Fil: Cross, Justin. No especifíca; Fil: Levin, Lonny R.. No especifíca; Fil: Buck, Jochen. No especifíca; Fil: Visconti, Pablo E.. University of Massachussets; Estados Unidos |
| description |
Mammalian sperm must undergo capacitation to become fertilization-competent. While working on mice, we recently developed a new methodology for treating sperm in vitro, which results in higher rates of fertilization and embryo development after in vitro fertilization. Sperm incubated in media devoid of nutrients lose motility, although they remain viable. Upon re-adding energy substrates, sperm resume motility and become capacitated with improved functionality. Here, we explore how sperm energy restriction and recovery (SER) treatment affects sperm metabolism and capacitation-associated signaling. Using extracellular flux analysis and metabolite profiling and tracing via nuclear magnetic resonance (NMR) and mass spectrometry (MS), we found that the levels of many metabolites were altered during the starvation phase of SER. Of particular interest, two metabolites, AMP and L-carnitine, were significantly increased in energy-restricted sperm. Upon re-addition of glucose and initiation of capacitation, most metabolite levels recovered and closely mimic the levels observed in capacitating sperm that have not undergone starvation. In both control and SER-treated sperm, incubation under capacitating conditions upregulated glycolysis and oxidative phosphorylation. However, ATP levels were diminished, presumably reflecting the increased energy consumption during capacitation. Flux data following the fate of 13C glucose indicate that, similar to other cells with high glucose consumption rates, pyruvate is converted into 13C-lactate and, with lower efficiency, into 13C-acetate, which are then released into the incubation media. Furthermore, our metabolic flux data show that exogenously supplied glucose is converted into citrate, providing evidence that in sperm cells, as in somatic cells, glycolytic products can be converted into Krebs cycle metabolites. |
| publishDate |
2023 |
| dc.date.none.fl_str_mv |
2023-08 |
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info:eu-repo/semantics/article info:eu-repo/semantics/publishedVersion http://purl.org/coar/resource_type/c_6501 info:ar-repo/semantics/articulo |
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article |
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publishedVersion |
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http://hdl.handle.net/11336/244026 Romarowski, Ana; Fejzo, Jasna; Nayyab, Saman; Martín Hidalgo, David; Gervasi, Maria Gracia; et al.; Mouse sperm energy restriction and recovery (SER) revealed novel metabolic pathways; Frontiers Media; Frontiers in Cell and Developmental Biology; 11; 8-2023; 1-18 2296-634X CONICET Digital CONICET |
| url |
http://hdl.handle.net/11336/244026 |
| identifier_str_mv |
Romarowski, Ana; Fejzo, Jasna; Nayyab, Saman; Martín Hidalgo, David; Gervasi, Maria Gracia; et al.; Mouse sperm energy restriction and recovery (SER) revealed novel metabolic pathways; Frontiers Media; Frontiers in Cell and Developmental Biology; 11; 8-2023; 1-18 2296-634X CONICET Digital CONICET |
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eng |
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eng |
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Frontiers Media |
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