Inheritable testicular metabolic memory of high-fat diet causes transgenerational sperm defects in mice
The consumption of energy-dense diets has contributed to an increase in the prevalence of obesity and its comorbidities worldwide. The adoption of unhealthy feeding habits often occurs at early age, prompting the early onset of metabolic disease with unknown consequences for reproductive function la...
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| Veröffentlicht in: | Scientific reports 2021-05, Vol.11 (1), p.9444-15, Article 9444 |
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| creator | Crisóstomo, Luís Jarak, Ivana Rato, Luís P. Raposo, João F. Batterham, Rachel L. Oliveira, Pedro F. Alves, Marco G. |
| description | The consumption of energy-dense diets has contributed to an increase in the prevalence of obesity and its comorbidities worldwide. The adoption of unhealthy feeding habits often occurs at early age, prompting the early onset of metabolic disease with unknown consequences for reproductive function later in life. Recently, evidence has emerged regarding the intergenerational and transgenerational effects of high-fat diets (HFD) on sperm parameters and testicular metabolism. Hereby, we study the impact of high-fat feeding male mice (F
0
) on the testicular metabolome and function of their sons (F
1
) and grandsons (F
2
). Testicular content of metabolites related to insulin resistance, cell membrane remodeling, nutritional support and antioxidative stress (leucine, acetate, glycine, glutamine, inosine) were altered in sons and grandsons of mice fed with HFD, comparing to descendants of chow-fed mice. Sperm counts were lower in the grandsons of mice fed with HFD, even if transient. Sperm quality was correlated to testicular metabolite content in all generations. Principal Component Analysis of sperm parameters and testicular metabolites revealed an HFD-related phenotype, especially in the diet-challenged generation and their grandsons. Ancestral HFD, even if transient, causes transgenerational “inherited metabolic memory” in the testicular tissue, characterized by changes in testicular metabolome and function. |
| doi_str_mv | 10.1038/s41598-021-88981-3 |
| format | Article |
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0
) on the testicular metabolome and function of their sons (F
1
) and grandsons (F
2
). Testicular content of metabolites related to insulin resistance, cell membrane remodeling, nutritional support and antioxidative stress (leucine, acetate, glycine, glutamine, inosine) were altered in sons and grandsons of mice fed with HFD, comparing to descendants of chow-fed mice. Sperm counts were lower in the grandsons of mice fed with HFD, even if transient. Sperm quality was correlated to testicular metabolite content in all generations. Principal Component Analysis of sperm parameters and testicular metabolites revealed an HFD-related phenotype, especially in the diet-challenged generation and their grandsons. Ancestral HFD, even if transient, causes transgenerational “inherited metabolic memory” in the testicular tissue, characterized by changes in testicular metabolome and function.</description><identifier>ISSN: 2045-2322</identifier><identifier>EISSN: 2045-2322</identifier><identifier>DOI: 10.1038/s41598-021-88981-3</identifier><identifier>PMID: 33941835</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/136/2442 ; 631/45/320 ; Acetic acid ; Cell membranes ; Diet ; Energy consumption ; Glutamine ; Glycine ; High fat diet ; Humanities and Social Sciences ; Insulin ; Insulin resistance ; Metabolic disorders ; Metabolism ; Metabolites ; multidisciplinary ; Nutrient deficiency ; Phenotypes ; Principal components analysis ; Science ; Science (multidisciplinary) ; Sperm ; Testes</subject><ispartof>Scientific reports, 2021-05, Vol.11 (1), p.9444-15, Article 9444</ispartof><rights>The Author(s) 2021</rights><rights>The Author(s) 2021. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c507t-e1259dcb9112fa90b1e16e8e835dd937cafba967ffd8d73a579a90f2031522043</citedby><cites>FETCH-LOGICAL-c507t-e1259dcb9112fa90b1e16e8e835dd937cafba967ffd8d73a579a90f2031522043</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8093209/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8093209/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,27903,27904,41099,42168,51554,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33941835$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Crisóstomo, Luís</creatorcontrib><creatorcontrib>Jarak, Ivana</creatorcontrib><creatorcontrib>Rato, Luís P.</creatorcontrib><creatorcontrib>Raposo, João F.</creatorcontrib><creatorcontrib>Batterham, Rachel L.</creatorcontrib><creatorcontrib>Oliveira, Pedro F.</creatorcontrib><creatorcontrib>Alves, Marco G.</creatorcontrib><title>Inheritable testicular metabolic memory of high-fat diet causes transgenerational sperm defects in mice</title><title>Scientific reports</title><addtitle>Sci Rep</addtitle><addtitle>Sci Rep</addtitle><description>The consumption of energy-dense diets has contributed to an increase in the prevalence of obesity and its comorbidities worldwide. The adoption of unhealthy feeding habits often occurs at early age, prompting the early onset of metabolic disease with unknown consequences for reproductive function later in life. Recently, evidence has emerged regarding the intergenerational and transgenerational effects of high-fat diets (HFD) on sperm parameters and testicular metabolism. Hereby, we study the impact of high-fat feeding male mice (F
0
) on the testicular metabolome and function of their sons (F
1
) and grandsons (F
2
). Testicular content of metabolites related to insulin resistance, cell membrane remodeling, nutritional support and antioxidative stress (leucine, acetate, glycine, glutamine, inosine) were altered in sons and grandsons of mice fed with HFD, comparing to descendants of chow-fed mice. Sperm counts were lower in the grandsons of mice fed with HFD, even if transient. Sperm quality was correlated to testicular metabolite content in all generations. Principal Component Analysis of sperm parameters and testicular metabolites revealed an HFD-related phenotype, especially in the diet-challenged generation and their grandsons. Ancestral HFD, even if transient, causes transgenerational “inherited metabolic memory” in the testicular tissue, characterized by changes in testicular metabolome and function.</description><subject>631/136/2442</subject><subject>631/45/320</subject><subject>Acetic acid</subject><subject>Cell membranes</subject><subject>Diet</subject><subject>Energy consumption</subject><subject>Glutamine</subject><subject>Glycine</subject><subject>High fat diet</subject><subject>Humanities and Social Sciences</subject><subject>Insulin</subject><subject>Insulin resistance</subject><subject>Metabolic disorders</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>multidisciplinary</subject><subject>Nutrient deficiency</subject><subject>Phenotypes</subject><subject>Principal components analysis</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Sperm</subject><subject>Testes</subject><issn>2045-2322</issn><issn>2045-2322</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNp9UUuLFDEQDqK4y7h_wIMEPLfmOZ1cBFl8DCx40XPIo9KTobszJt3C_nvj9rruXgwUKaq--urxIfSakneUcPW-Ciq16gijnVJa0Y4_Q5eMCNkxztjzR_4Fuqr1RNqTTAuqX6ILzpujuLxEw2E-QkmLdSPgBeqS_DragidooTwm37wpl1ucIz6m4dhFu-CQYMHerhUqXoqd6wAzFLukPNsR1zOUCQeI4JeK04yn5OEVehHtWOHq_t-hH58_fb_-2t18-3K4_njTeUn6pQPKpA7eaUpZtJo4CnQPCtqsIWjeexud1fs-xqBCz63sdUNFRjiVrG3Md-iw8YZsT-Zc0mTLrck2mbtALoOxpS05giGaCeui9ECpgCBdEM4JIZSNwpGeNK4PG9d5dRMED3NbdnxC-jQzp6MZ8i-jiOas2Q69vSco-efajmtOeS3tRtUwySjby71gDcU2lC-51gLxoQMl5o_WZtPaNK3NndaGt6I3j2d7KPmrbAPwDVBbah6g_Ov9H9rf4PO2zw</recordid><startdate>20210503</startdate><enddate>20210503</enddate><creator>Crisóstomo, Luís</creator><creator>Jarak, Ivana</creator><creator>Rato, Luís P.</creator><creator>Raposo, João F.</creator><creator>Batterham, Rachel L.</creator><creator>Oliveira, Pedro F.</creator><creator>Alves, Marco G.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><general>Nature Portfolio</general><scope>C6C</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20210503</creationdate><title>Inheritable testicular metabolic memory of high-fat diet causes transgenerational sperm defects in mice</title><author>Crisóstomo, Luís ; 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The adoption of unhealthy feeding habits often occurs at early age, prompting the early onset of metabolic disease with unknown consequences for reproductive function later in life. Recently, evidence has emerged regarding the intergenerational and transgenerational effects of high-fat diets (HFD) on sperm parameters and testicular metabolism. Hereby, we study the impact of high-fat feeding male mice (F
0
) on the testicular metabolome and function of their sons (F
1
) and grandsons (F
2
). Testicular content of metabolites related to insulin resistance, cell membrane remodeling, nutritional support and antioxidative stress (leucine, acetate, glycine, glutamine, inosine) were altered in sons and grandsons of mice fed with HFD, comparing to descendants of chow-fed mice. Sperm counts were lower in the grandsons of mice fed with HFD, even if transient. Sperm quality was correlated to testicular metabolite content in all generations. Principal Component Analysis of sperm parameters and testicular metabolites revealed an HFD-related phenotype, especially in the diet-challenged generation and their grandsons. Ancestral HFD, even if transient, causes transgenerational “inherited metabolic memory” in the testicular tissue, characterized by changes in testicular metabolome and function.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>33941835</pmid><doi>10.1038/s41598-021-88981-3</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | 631/136/2442 631/45/320 Acetic acid Cell membranes Diet Energy consumption Glutamine Glycine High fat diet Humanities and Social Sciences Insulin Insulin resistance Metabolic disorders Metabolism Metabolites multidisciplinary Nutrient deficiency Phenotypes Principal components analysis Science Science (multidisciplinary) Sperm Testes |
| title | Inheritable testicular metabolic memory of high-fat diet causes transgenerational sperm defects in mice |
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