Spire localization via zinc finger—containing domain is crucial for the asymmetric division of mouse oocyte

• Published in: The FASEB journal 2019-03, Vol.33 (3), p.4432-4447
• Main Authors: Jo, Yu-Jin, Lee, In-Won, Jung, Seung-Min, Kwon, Jeongwoo, Kim, Nam-Hyung, Namgoong, Suk
• Format: Article
• Language: English
• Subjects: Actin Cytoskeleton - physiology; Actin Cytoskeleton - ultrastructure; Amino Acid Sequence; Animals; Asymmetric Cell Division - physiology; asymmetric division; Cytokinesis; Cytoplasmic Vesicles - metabolism; Female; Formins - metabolism; Meiosis - physiology; Mice; Microfilament Proteins - antagonists & inhibitors; Microfilament Proteins - chemistry; Microfilament Proteins - genetics; Microfilament Proteins - physiology; Nerve Tissue Proteins - antagonists & inhibitors; Nerve Tissue Proteins - chemistry; Nerve Tissue Proteins - metabolism; Nerve Tissue Proteins - physiology; Oocytes - cytology; Oocytes - metabolism; Parthenogenesis - drug effects; Point Mutation; Protein Interaction Mapping; Protein Transport; Recombinant Proteins - genetics; Recombinant Proteins - metabolism; Sequence Alignment; Sequence Homology, Amino Acid; Soire; Sperm Injections, Intracytoplasmic; Spindle Apparatus - physiology; Spindle Apparatus - ultrastructure; Strontium - pharmacology; Zinc - physiology; zinc finger; Zinc Fingers - physiology
• ISSN: 0892-6638; 1530-6860
• DOI: 10.1096/fj.201801905R

ABSTRACT Zinc plays an essential role in mammalian oocyte maturation, fertilization, and early embryogenesis, and depletion of zinc impairs cell cycle control, asymmetric division, and cytokinesis in oocyte. We report that zinc, via the actin nucleator Spire, acts as an essential regulator of the actin cytoskeleton remodeling during mouse oocyte maturation and fertilization. Depletion of zinc in the mouse oocyte impaired cortical and cytoplasmic actin formation. Spire is colocalized with zinc‐containing vesicles via its zinc finger‐containing Fab1, YOTB, Vac 1, EEA1 (FYVE) domain. Improper localization of Spire by zinc depletion or mutations in the FYVE domain impair cytoplasmic actin mesh formations and asymmetric division and cytokinesis of oocyte. All 3 major domains of the Spire are required for its proper localization and activity. After fertilization or parthenogenetic activation, Spire localization was dramatically altered following zinc release from the oocyte. Collectively, our data reveal novel roles for zinc in the regulation of the actin nucleator Spire by controlling its localization in mammalian oocyte.—Jo, Y.‐J., Lee, I.‐W., Jung, S.‐M., Kwon, J., Kim, N.‐H., Namgoong, S. Spire localization via zinc finger—containing domain is crucial for the asymmetric division of mouse oocyte. FASEB J. 33, 4432–4447 (2019). www.fasebj.org