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Human sperm displays rapid responses to diet
Linköping University, Faculty of Medicine and Health Sciences. Linköping University, Department of Clinical and Experimental Medicine, Divison of Neurobiology.ORCID iD: 0000-0001-9182-9401
Linköping University, Faculty of Medicine and Health Sciences. Linköping University, Department of Clinical and Experimental Medicine, Divison of Neurobiology.
Josep Carreras Leukaemia Res Inst IJC, Spain.
Linköping University, Department of Clinical and Experimental Medicine, Division of Children's and Women's health. Linköping University, Faculty of Medicine and Health Sciences. Region Östergötland, Center of Paediatrics and Gynaecology and Obstetrics, Department of Gynaecology and Obstetrics in Linköping.
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2019 (English)In: PLoS biology, ISSN 1544-9173, E-ISSN 1545-7885, Vol. 17, no 12, article id e3000559Article in journal (Refereed) Published
Abstract [en]

The global rise in obesity and steady decline in sperm quality are two alarming trends that have emerged during recent decades. In parallel, evidence from model organisms shows that paternal diet can affect offspring metabolic health in a process involving sperm tRNA-derived small RNA (tsRNA). Here, we report that human sperm are acutely sensitive to nutrient flux, both in terms of sperm motility and changes in sperm tsRNA. Over the course of a 2-week diet intervention, in which we first introduced a healthy diet followed by a diet rich in sugar, sperm motility increased and stabilized at high levels. Small RNA-seq on repeatedly sampled sperm from the same individuals revealed that tsRNAs were up-regulated by eating a high-sugar diet for just 1 week. Unsupervised clustering identified two independent pathways for the biogenesis of these tsRNAs: one involving a novel class of fragments with specific cleavage in the T-loop of mature nuclear tRNAs and the other exclusively involving mitochondrial tsRNAs. Mitochondrial involvement was further supported by a similar up-regulation of mitochondrial rRNA-derived small RNA (rsRNA). Notably, the changes in sugar-sensitive tsRNA were positively associated with simultaneous changes in sperm motility and negatively associated with obesity in an independent clinical cohort. This rapid response to a dietary intervention on tsRNA in human sperm is attuned with the paternal intergenerational metabolic responses found in model organisms. More importantly, our findings suggest shared diet-sensitive mechanisms between sperm motility and the biogenesis of tsRNA, which provide novel insights about the interplay between nutrition and male reproductive health.

Place, publisher, year, edition, pages
San Francisco, CA United States: PUBLIC LIBRARY SCIENCE , 2019. Vol. 17, no 12, article id e3000559
National Category
Biochemistry Molecular Biology
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URN: urn:nbn:se:liu:diva-163216DOI: 10.1371/journal.pbio.3000559ISI: 000506151200001PubMedID: 31877125Scopus ID: 2-s2.0-85077267216OAI: oai:DiVA.org:liu-163216DiVA, id: diva2:1391025
Note

Funding Agencies|Swedish Research CouncilSwedish Research Council [201503141]; Knut and Alice Wallenberg FoundationKnut & Alice Wallenberg Foundation [2015.0165]; Strategic Research Area Health Care Science at Karolinska Institutet/Umea University; Ragnar Soderberg

Available from: 2020-02-03 Created: 2020-02-03 Last updated: 2025-02-20Bibliographically approved

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Nätt, DanielÖrtegren Kugelberg, UnnNedstrand, ElizabethZalavary, StefanHenriksson, PontusNijm, CarolaJaderquist, JuliaSandborg, JohannaFlinke Carlsson, EvaRamesh, RashmiÖrkenby, LovisaAppelkvist, FilipLingg, ThomasLöf, MarieÖst, Anita
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Faculty of Medicine and Health SciencesDivison of NeurobiologyDivision of Children's and Women's healthDepartment of Gynaecology and Obstetrics in LinköpingDivision of Community Medicine
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