Developmental changes in nuclear lamina components during germ cell differentiation

ABSTRACT

The nuclear lamina (NL) changes composition for regulation of nuclear events. We investigated changes that occur in Drosophila oogenesis, revealing switches in NL composition during germ cell differentiation. Germline stem cells (GSCs) express only LamB and predominantly emerin, whereas differentiating nurse cells predominantly express LamC and emerin2. A change in LamC-specific localization also occurs, wherein phosphorylated LamC redistributes to the nuclear interior only in the oocyte, prior to transcriptional reactivation of the meiotic genome. These changes support existing concepts that LamC promotes differentiation, a premise that was tested. Remarkably ectopic LamC production in GSCs did not promote premature differentiation. Increased LamC levels in differentiating germ cells altered internal nuclear structure, increased RNA production, and reduced female fertility due to defects in eggshell formation. These studies suggest differences between Drosophila lamins are regulatory, not functional, and reveal an unexpected robustness to level changes of a major scaffolding component of the NL.

KEYWORDS:

• Drosophila oogenesis
• emerin
• LEM domain proteins
• nuclear structure
• operculum
• otefin
• phosphorylated lamin
• stem cell homeostasis

Acknowledgments

We thank Nicholas Lyon for technical assistance in the production of the UASp-lamC transgene, Tingting Duan for both technical assistance and training laboratory members, and members of the Geyer laboratory and Lacy Barton (University of Texas, San Antonio) for helpful discussions.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Author contributions

Conceptualization, I.E.P. and P.K.G.; methodology, I.E.P., S.D.J., and P.K.G.; investigation, I.E.P., S.D.J., K.M.P.; Data curation, I.E.P., S.D.J., K.M.P; original draft, P.K.G., review and editing I.E.P., S.D.J., K.M.P. and P.K.G.; funding acquisition, P.K.G.; supervision, P.K.G.

Data availability statement

The Drosophila strains are available upon request. The data that support the findings of this study are openly available in https://doi.org/10.6084/m9.figshare.25250224. Supplemental files are published at figshare https://doi.org/10.6084/m9.figshare.25250224.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/19491034.2024.2339214

Additional information

Funding

This work was supported by the National Institute of Health GM087341 to P.K.G.