Postmitotic annulate lamellae assembly contributes to nuclear envelope reconstitution in daughter cells

Abstract

Edited by Xiao-Fan Wang In higher eukaryotic cells, the nuclear envelope (NE) is composed of double nuclear membranes studded with nuclear pore complexes (NPCs) and undergoes dynamic disassembly and reassembly during the cell cycle. However, how the NE and NPC reassemble remains largely unclear. Here, using HeLa, HEK293, and Drosophila cells, along with immunofluorescence microscopy and transmission EM methods, we found that postmitotic annulate lamellae (AL) assembly contributes to NE and NPC assembly. We observed that the AL are parallel membrane-pair stacks and possess regularly spaced AL pore complexes (ALPCs) that are morphologically similar to the NPCs. We found that the AL assemble in the cytoplasm during mitotic exit simultaneously with NE reformation in daughter cells. Then, the assembled AL either bound the decondensing chromatin to directly transform into the NE or bound and fused with the outer nuclear membrane to join the assembling NE. The AL did not colocalize with sheet and tubular endoplasmic reticulum (ER) marker proteins on the ER or the lamin B receptor-localized membrane in the cytoplasm, suggesting that postmitotic AL assembly occurs independently of the chromatin and ER. Collectively, our results indicate that postmitotic AL assembly is a common cellular event and an intermediate step in NE and NPC assembly and in NE expansion in higher eukaryotic cells.

The coordination of nuclear envelope assembly and chromosome segregation in metazoans

“…Whether this association of ELYS with annulate lamellae is then followed by ELYS chromatin-binding to trigger subsequent full NPC assembly remains to be determined. Nevertheless, it is appealing to speculate this process may share some common features with the postmitotic NPC assembly mechanism in normal somatic cells [62]. In summary, the recruitment of the nuclear membrane and NPCs to chromatin are tightly coordinated during mitotic exit to enable the rapid formation of a functional nucleus.…”

Annulate lamellae and intracellular pathogens

“…m, mitochondria; ld, lipid droplet as the area of the nuclear envelope increases, occurs rapidly (within 1-2 min), due to the insertion of large portions of AL membranes rather than individual nuclear pores (De Magistris & Antonin, 2018;Hampoelz et al, 2016). This mechanism has also recently been observed in other cell types, suggesting that it may be common to all proliferating eukaryotic cells (Ren et al, 2019).…”

Mitotic disassembly and reassembly of nuclear pore complexes

“…How this works mechanistically is not understood. A similar process was recently suggested to contribute to (post)-mitotic NPC assembly in mammalian somatic cells; however, direct recruitment of ALs to the nucleus was not unambiguously shown [84]. In Drosophila embryos, the AL-based mode only operates before gastrulation in absence of LBR, which prevents this mode later in development [83].…”