Mitochondrial Function and Regulation in Spermatogenesis and Activation of Caenorhabditis elegans
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1)MOE Key Laboratory of Cell Proliferation and Regulation Biology, College of Life Sciences, Beijing Normal University, Beijing 100875, China;2)College of Life Science and Food Engineering, Fuyang Normal University, Fuyang 236037, China;3)Key Laboratory of RNA Biology, CAS Center for Excellence in Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China;4)College of Life Science, University of Chinese Academy of Sciences, Beijing 100049, China

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This work was supported by grants from National Key Research and Development Plan (2023YFA1801100) and The National Natural Science Foundation of China (32270774).

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    Abstract:

    Mitochondria play a pivotal role in spermatogenesis and sperm activation in Caenorhabditis elegans, serving as the primary ATP supplier for cell division and differentiation while also acting as a key regulator of zinc ion homeostasis, membrane dynamics, and apoptotic signaling. This review systematically summarizes the essential mitochondrial mechanisms at different stages of sperm development, highlighting their multifaceted contributions beyond energy metabolism. Mitochondria are crucial for maintaining the health and stability of the gonads by regulating key apoptotic execution proteins that facilitate the proper elimination of damaged or unnecessary germ cells. Additionally, mitochondria dynamically adjust their energy supply to meet the metabolic demands of different stages of germline development. During early spermatogenesis, mitochondria provide ATP to fuel mitotic and meiotic divisions, support cellular differentiation, and regulate H+ and Zn2+ exchange to maintain cytoplasmic homeostasis, thereby ensuring the proper maturation and functionality of sperm cells. As spermatogenesis progresses, mitochondria participate in processing and sorting essential sperm proteins, such as major sperm protein (MSP), and contribute to the formation of membranous organelles (MOs), which are critical for subsequent activation events. During sperm activation, mitochondria play a dual role in ensuring a successful transition from immotile spermatids to fully functional spermatozoa. First, they provide ATP to facilitate pseudopod formation, MO fusion, and ion channel regulation, all of which are essential for sperm motility and fertilization potential. Second, mitochondria regulate the quality and quantity of functional mitochondria within sperm cells through mitopherogenesis—a recently discovered process in which mitochondrial vesicles are selectively released, ensuring that only healthy mitochondria are retained. This quality-control mechanism optimizes mitochondrial function, which is crucial for sustaining sperm motility and longevity. Beyond their traditional role in energy metabolism, mitochondria may also contribute to protein synthesis during spermatogenesis and activation. Recent evidence suggests that mitochondrial ribosomes actively translate specific proteins required for sperm function, challenging the long-standing belief that spermatozoa do not engage in de novo protein synthesis after differentiation. This emerging perspective raises important questions about the role of mitochondria in regulating sperm activation at the molecular level, particularly in modulating oxidative phosphorylation (OXPHOS) protein composition to optimize ATP production. In summary, mitochondria serve as both the central energy hub and a crucial regulatory factor in sperm activation, metabolic homeostasis, and reproductive success. Their involvement extends beyond ATP generation to include apoptotic regulation, ion homeostasis, vesicle-mediated mitochondrial quality control, and potential contributions to protein synthesis. Understanding these mitochondrial functions in C. elegans not only deepens our knowledge of nematode reproductive biology, but also provides valuable insights into broader mechanisms governing mitochondrial regulation in germline cells across species. These findings open new avenues for future research into the interplay between mitochondria, energy metabolism, and sperm function, with potential implications for reproductive health and fertility studies.

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CHANG Zhan-Xin, MIAO Long, WANG Peng. Mitochondrial Function and Regulation in Spermatogenesis and Activation of Caenorhabditis elegans[J]. Progress in Biochemistry and Biophysics,,():

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History
  • Received:December 24,2024
  • Revised:April 03,2025
  • Accepted:March 07,2025
  • Online: March 07,2025
  • Published: