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
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/244026

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network_name_str CONICET Digital (CONICET)
spelling 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
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
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info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv 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
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/journals/cell-and-developmental-biology/articles/10.3389/fcell.2023.1234221/full
info:eu-repo/semantics/altIdentifier/doi/10.3389/fcell.2023.1234221
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
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instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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