» Articles » PMID: 33558389

The Intrinsically Disordered Protein SPE-18 Promotes Localized Assembly of MSP in Spermatocytes

Overview
Journal Development
Specialty Biology
Date 2021 Feb 9
PMID 33558389
Citations 5
Authors
Affiliations
Soon will be listed here.
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 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.

Citing Articles

RNAi-dependent expression of sperm genes in ADL chemosensory neurons is required for olfactory responses in .

Ow M, Nishiguchi M, Dar A, Butcher R, Hall S Front Mol Biosci. 2024; 11:1396587.

PMID: 39055986 PMC: 11269235. DOI: 10.3389/fmolb.2024.1396587.


Active learning of the thermodynamics-dynamics trade-off in protein condensates.

An Y, Webb M, Jacobs W Sci Adv. 2024; 10(1):eadj2448.

PMID: 38181073 PMC: 10775998. DOI: 10.1126/sciadv.adj2448.


NHR-23 and SPE-44 regulate distinct sets of genes during Caenorhabditis elegans spermatogenesis.

Ragle J, Morrison K, Vo A, Johnson Z, Hernandez Lopez J, Rechtsteiner A G3 (Bethesda). 2022; 12(11).

PMID: 36135804 PMC: 9635660. DOI: 10.1093/g3journal/jkac256.


Subcellular patterns of SPE-6 localization reveal unexpected complexities in Caenorhabditis elegans sperm activation and sperm function.

Peterson J, Tocheny C, Prajapati G, LaMunyon C, Shakes D G3 (Bethesda). 2021; 11(11).

PMID: 34849789 PMC: 8527485. DOI: 10.1093/g3journal/jkab288.


MFP1/MSD-1 and MFP2/NSPH-2 co-localize with MSP during spermatogenesis.

Morrison K, Uyehara C, Ragle J, Ward J, Shakes D MicroPubl Biol. 2021; 2021.

PMID: 34316545 PMC: 8299296. DOI: 10.17912/micropub.biology.000427.

References
1.
Nelson G, Roberts T, Ward S . Caenorhabditis elegans spermatozoan locomotion: amoeboid movement with almost no actin. J Cell Biol. 1982; 92(1):121-31. PMC: 2111997. DOI: 10.1083/jcb.92.1.121. View

2.
Roberts T . Major sperm protein. Curr Biol. 2005; 15(5):R153. DOI: 10.1016/j.cub.2005.02.036. View

3.
Ishida T, Kinoshita K . PrDOS: prediction of disordered protein regions from amino acid sequence. Nucleic Acids Res. 2007; 35(Web Server issue):W460-4. PMC: 1933209. DOI: 10.1093/nar/gkm363. View

4.
Svitkina T . Ultrastructure of the actin cytoskeleton. Curr Opin Cell Biol. 2018; 54:1-8. PMC: 6103910. DOI: 10.1016/j.ceb.2018.02.007. View

5.
Reinke V, Smith H, NANCE J, Wang J, Van Doren C, Begley R . A global profile of germline gene expression in C. elegans. Mol Cell. 2000; 6(3):605-16. DOI: 10.1016/s1097-2765(00)00059-9. View