ArticleProceedings of the National Academy of Sciences of the United States of America2016
Autophagy and ubiquitin-proteasome system contribute to sperm mitophagy after mammalian fertilization.
Article in Proceedings of the National Academy of Sciences of the United States of America, 2016. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 84 papers, 2 of them syntheses that pooled it.
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Who cites it
84 citing papers in PubMed, 2 syntheses or guidelines pooled it, 173 citations in OpenAlex.
- Pooled it
- Guidelines for the use and interpretation of assays for monitoring autophagy (4th edition)Autophagy · 2021Guideline
- Monitoring the fate of paternal mitochondria and their elimination in rice zygotes.Plant physiology · 2026Article
- Phenotyping of post-fertilization sperm mitophagy determinants discovered in a mammalian gamete-based cell-free system.Biological research · 2026Article
- Nuclear Transfer Perturbs Genomic Balance.Epigenomes · 2026Article
- CCDC41 Drives Oocyte Meiotic Progression by Promoting Rab11a/Rab7-Positive Vesicle Fusion with Target Membranes.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2026Article
- The nuclear and mitochondrial genomes need to tango. How is their dance synchronized during development?NAR molecular medicine · 2026Article
- Autophagy-Related Proteins Influence Mouse Epididymal Sperm Motility.International journal of molecular sciences · 2025Article
- Mitochondrial curation for the next generation.Current opinion in genetics & development · 2025Review
- Interplay of Oxidative Stress, Autophagy, and Rubicon in Ovarian Follicle Dynamics: Orchestrating Ovarian Aging.Antioxidants (Basel, Switzerland) · 2025Review
- A nuclear-encoded endonuclease governs the paternal transmission of mitochondria in Cucumis plants.Nature communications · 2025Article
- Cytoplasmic inheritance: The transmission of plastid and mitochondrial genomes across cells and generations.Plant physiology · 2025Review
- Can the Supplementation of Oocytes with Extra Copies of mtDNA Impact Development Without Being Transmitted? A Molecular Account.International journal of molecular sciences · 2025Article
- Proteostasis as a Sentry for Sperm Quality and Male Fertility.Advances in experimental medicine and biology · 2025Review
- VPS28 regulates triglyceride synthesis via ubiquitination in bovine mammary epithelial cells.Scientific reports · 2024Article
- Autophagy in reproduction and pregnancy-associated diseases.iScience · 2024Review
- Supplementation of Oocytes by Microinjection with Extra Copies of mtDNA Alters Metabolite Profiles and Interactions with Expressed Genes in a Tissue-Specific Manner.Biomolecules · 2024Article
- Bottom-up approach to deciphering the targets of the ubiquitin-proteasome system in porcine sperm capacitation.Scientific reports · 2024Article
- Dual role of valosin-containing protein (VCP/p97) in mouse sperm during capacitation.Reproduction (Cambridge, England) · 2024Article
- Endonuclease G is dispensable for sperm mitochondrial DNA elimination during spermatogenesis in mice.Biology open · 2024Article
24 more citing papers are in PubMed but not listed here.
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Authors and funding
5 authors at 3 institutions in 1 country.
Funding
Abstract
Maternal inheritance of mitochondria and mtDNA is a universal principle in human and animal development, guided by selective ubiquitin-dependent degradation of the sperm-borne mitochondria after fertilization. However, it is not clear how the 26S proteasome, the ubiquitin-dependent protease that is only capable of degrading one protein molecule at a time, can dispose of a whole sperm mitochondrial sheath. We hypothesized that the canonical ubiquitin-like autophagy receptors [sequestosome 1 (SQSTM1), microtubule-associated protein 1 light chain 3 (LC3), gamma-aminobutyric acid receptor-associated protein (GABARAP)] and the nontraditional mitophagy pathways involving ubiquitin-proteasome system and the ubiquitin-binding protein dislocase, valosin-containing protein (VCP), may act in concert during mammalian sperm mitophagy. We found that the SQSTM1, but not GABARAP or LC3, associated with sperm mitochondria after fertilization in pig and rhesus monkey zygotes. Three sperm mitochondrial proteins copurified with the recombinant, ubiquitin-associated domain of SQSTM1. The accumulation of GABARAP-containing protein aggregates was observed in the vicinity of sperm mitochondrial sheaths in the zygotes and increased in the embryos treated with proteasomal inhibitor MG132, in which intact sperm mitochondrial sheaths were observed. Pharmacological inhibition of VCP significantly delayed the process of sperm mitophagy and completely prevented it when combined with microinjection of autophagy-targeting antibodies specific to SQSTM1 and/or GABARAP. Sperm mitophagy in higher mammals thus relies on a combined action of SQSTM1-dependent autophagy and VCP-mediated dislocation and presentation of ubiquitinated sperm mitochondrial proteins to the 26S proteasome, explaining how the whole sperm mitochondria are degraded inside the fertilized mammalian oocytes by a protein recycling system involved in degradation of single protein molecules.
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