RRC ID 65396
Author Price KL, Presler M, Uyehara CM, Shakes DC.
Title The intrinsically disordered protein SPE-18 promotes localized assembly of MSP in Caenorhabditis elegans spermatocytes.
Journal Development
Abstract Many specialized cells use unconventional strategies of cytoskeletal control. Nematode spermatocytes discard their actin and tubulin following meiosis, and instead employ the regulated assembly/disassembly of the Major Sperm Protein (MSP) to drive sperm motility. However, prior to the meiotic divisions, MSP is sequestered through its assembly into paracrystalline structures called fibrous bodies (FBs). The accessory proteins that direct this sequestration process have remained mysterious. This study reveals SPE-18 as an intrinsically disordered protein that is essential for MSP assembly within FBs. In spe-18 mutant spermatocytes, MSP forms disorganized cortical fibers, and the cells arrest in meiosis without forming haploid sperm. In wild-type spermatocytes, SPE-18 localizes to pre-FB complexes and functions with the kinase SPE-6 to localize MSP assembly. Changing patterns of SPE-18 localization uncover previously unappreciated complexities in FB maturation. Later, within newly individualized spermatids, SPE-18 is rapidly lost, yet SPE-18 loss alone is insufficient for MSP disassembly. Our findings reveal an alternative strategy for sequestering cytoskeletal elements, not as monomers but in localized, bundled polymers. Additionally, these studies provide an important example of disordered proteins promoting ordered cellular structures.
Volume 148(5)
Published 2021-3-5
DOI 10.1242/dev.195875
PII dev.195875
PMID 33558389
PMC PMC7938801
MeSH Amino Acid Sequence Animals Caenorhabditis elegans Caenorhabditis elegans Proteins / chemistry Caenorhabditis elegans Proteins / genetics Caenorhabditis elegans Proteins / metabolism* Cell Cycle Checkpoints Cytoskeleton / metabolism Intrinsically Disordered Proteins / chemistry Intrinsically Disordered Proteins / genetics Intrinsically Disordered Proteins / metabolism* Male Meiosis Mutagenesis Sequence Alignment Spermatids / metabolism Spermatocytes / cytology Spermatocytes / growth & development Spermatocytes / metabolism* Spermatogenesis