Nuclear Envelope Budding and Its Cellular Functions

Overview

Journal Nucleus

Date 2023 Feb 23

PMID 36814098

Authors

Katharina S Keuenhof

Verena Kohler

Filomena Broeskamp

Dimitra Panagaki

Sean D Speese

Sabrina Buttner

Johanna L Hoog

Affiliations

Soon will be listed here.

Abstract

The nuclear pore complex (NPC) has long been assumed to be the sole route across the nuclear envelope, and under normal homeostatic conditions it is indeed the main mechanism of nucleo-cytoplasmic transport. However, it has also been known that e.g. herpesviruses cross the nuclear envelope utilizing a pathway entitled nuclear egress or envelopment/de-envelopment. Despite this, a thread of observations suggests that mechanisms similar to viral egress may be transiently used also in healthy cells. It has since been proposed that mechanisms like nuclear envelope budding (NEB) can facilitate the transport of RNA granules, aggregated proteins, inner nuclear membrane proteins, and mis-assembled NPCs. Herein, we will summarize the known roles of NEB as a physiological and intrinsic cellular feature and highlight the many unanswered questions surrounding these intriguing nuclear events.

Citing Articles

Nuclear Structure, Size Regulation, and Role in Cell Migration.

Li Y, Ge S, Liu J, Sun D, Xi Y, Chen P Cells. 2025; 13(24.

PMID: 39768219 PMC: 11675058. DOI: 10.3390/cells13242130.

CLCC1 promotes membrane fusion during herpesvirus nuclear egress.

Dai B, Polack L, Sperl A, Dame H, Huynh T, Deveney C bioRxiv. 2024; .

PMID: 39386602 PMC: 11463520. DOI: 10.1101/2024.09.23.614151.

TorsinA is essential for neuronal nuclear pore complex localization and maturation.

Kim S, Phan S, Tran H, Shaw T, Shahmoradian S, Ellisman M Nat Cell Biol. 2024; 26(9):1482-1495.

PMID: 39117796 PMC: 11542706. DOI: 10.1038/s41556-024-01480-1.

Nuclear envelope budding: Getting large macromolecular complexes out of the nucleus.

Sule K, Nakamura M, Parkhurst S Bioessays. 2023; 46(2):e2300182.

PMID: 38044581 PMC: 10843589. DOI: 10.1002/bies.202300182.

The dynamic nuclear envelope: resilience in health and dysfunction in disease.

Turkmen A, Saik N, Ullman K Curr Opin Cell Biol. 2023; 85:102230.

PMID: 37660480 PMC: 10843620. DOI: 10.1016/j.ceb.2023.102230.

References

Zhang X, Chen S, Yoo S, Chakrabarti S, Zhang T, Ke T . Mutation in nuclear pore component NUP155 leads to atrial fibrillation and early sudden cardiac death. Cell. 2008; 135(6):1017-27. DOI: 10.1016/j.cell.2008.10.022. View

Lusk C, Colombi P . Toward a consensus on the mechanism of nuclear pore complex inheritance. Nucleus. 2014; 5(2):97-102. PMC: 4049925. DOI: 10.4161/nucl.28314. View

Reichelt R, Holzenburg A, Buhle Jr E, Jarnik M, Engel A, Aebi U . Correlation between structure and mass distribution of the nuclear pore complex and of distinct pore complex components. J Cell Biol. 1990; 110(4):883-94. PMC: 2116066. DOI: 10.1083/jcb.110.4.883. View

Ahmad I, Wilson D . HSV-1 Cytoplasmic Envelopment and Egress. Int J Mol Sci. 2020; 21(17). PMC: 7503644. DOI: 10.3390/ijms21175969. View

Klupp B, Granzow H, Mettenleiter T . Primary envelopment of pseudorabies virus at the nuclear membrane requires the UL34 gene product. J Virol. 2000; 74(21):10063-73. PMC: 102045. DOI: 10.1128/jvi.74.21.10063-10073.2000. View

Fradkin L, Budnik V . This bud's for you: mechanisms of cellular nucleocytoplasmic trafficking via nuclear envelope budding. Curr Opin Cell Biol. 2016; 41:125-31. PMC: 5019485. DOI: 10.1016/j.ceb.2016.05.001. View

Freibaum B, Lu Y, Lopez-Gonzalez R, Kim N, Almeida S, Lee K . GGGGCC repeat expansion in C9orf72 compromises nucleocytoplasmic transport. Nature. 2015; 525(7567):129-33. PMC: 4631399. DOI: 10.1038/nature14974. View

Fernandez-Martinez J, Rout M . Nuclear pore complex biogenesis. Curr Opin Cell Biol. 2009; 21(4):603-12. PMC: 2749478. DOI: 10.1016/j.ceb.2009.05.001. View

Li Y, Hassinger L, Thomson T, Ding B, Ashley J, Hassinger W . Lamin Mutations Accelerate Aging via Defective Export of Mitochondrial mRNAs through Nuclear Envelope Budding. Curr Biol. 2016; 26(15):2052-2059. PMC: 4999898. DOI: 10.1016/j.cub.2016.06.007. View

10.

Liu J, Hetzer M . Nuclear pore complex maintenance and implications for age-related diseases. Trends Cell Biol. 2021; 32(3):216-227. DOI: 10.1016/j.tcb.2021.10.001. View

11.

DeGrasse J, DuBois K, Devos D, Siegel T, Sali A, Field M . Evidence for a shared nuclear pore complex architecture that is conserved from the last common eukaryotic ancestor. Mol Cell Proteomics. 2009; 8(9):2119-30. PMC: 2742445. DOI: 10.1074/mcp.M900038-MCP200. View

12.

Richardson W, Mills A, Dilworth S, Laskey R, Dingwall C . Nuclear protein migration involves two steps: rapid binding at the nuclear envelope followed by slower translocation through nuclear pores. Cell. 1988; 52(5):655-64. DOI: 10.1016/0092-8674(88)90403-5. View

13.

Allegretti M, Zimmerli C, Rantos V, Wilfling F, Ronchi P, Fung H . In-cell architecture of the nuclear pore and snapshots of its turnover. Nature. 2020; 586(7831):796-800. DOI: 10.1038/s41586-020-2670-5. View

14.

Toyama B, Savas J, Park S, Harris M, Ingolia N, Yates 3rd J . Identification of long-lived proteins reveals exceptional stability of essential cellular structures. Cell. 2013; 154(5):971-982. PMC: 3788602. DOI: 10.1016/j.cell.2013.07.037. View

15.

Liu K, Shyu Y, Barbaro B, Lin Y, Chern Y, Thompson L . Disruption of the nuclear membrane by perinuclear inclusions of mutant huntingtin causes cell-cycle re-entry and striatal cell death in mouse and cell models of Huntington's disease. Hum Mol Genet. 2014; 24(6):1602-16. PMC: 4381756. DOI: 10.1093/hmg/ddu574. View

16.

de Castro I, Lusic M . Navigating through the nucleus with a virus. Curr Opin Genet Dev. 2019; 55:100-105. DOI: 10.1016/j.gde.2019.07.001. View

17.

Lucifora J, Delphin M . Current knowledge on Hepatitis Delta Virus replication. Antiviral Res. 2020; 179:104812. DOI: 10.1016/j.antiviral.2020.104812. View

18.

Roller R, Baines J . Herpesvirus Nuclear Egress. Adv Anat Embryol Cell Biol. 2017; 223:143-169. DOI: 10.1007/978-3-319-53168-7_7. View

19.

Roller R, Bjerke S, Haugo A, Hanson S . Analysis of a charge cluster mutation of herpes simplex virus type 1 UL34 and its extragenic suppressor suggests a novel interaction between pUL34 and pUL31 that is necessary for membrane curvature around capsids. J Virol. 2010; 84(8):3921-34. PMC: 2849510. DOI: 10.1128/JVI.01638-09. View

20.

Reynolds A, Wills E, Roller R, Ryckman B, Baines J . Ultrastructural localization of the herpes simplex virus type 1 UL31, UL34, and US3 proteins suggests specific roles in primary envelopment and egress of nucleocapsids. J Virol. 2002; 76(17):8939-52. PMC: 136992. DOI: 10.1128/jvi.76.17.8939-8952.2002. View