Coupling Lipid Synthesis with Nuclear Envelope Remodeling

Overview

Journal Trends Biochem Sci

Specialty Biochemistry

Date 2021 Sep 24

PMID 34556392

Citations 21

Authors

Sarah R Barger

Lauren Penfield

Shirin Bahmanyar

Affiliations

Soon will be listed here.

Abstract

The nuclear envelope (NE) is a protective barrier to the genome, yet its membranes undergo highly dynamic remodeling processes that are necessary for cell growth and maintenance. While mechanisms by which proteins promote NE remodeling are emerging, the types of bilayer lipids and the lipid-protein interactions that define and sculpt nuclear membranes remain elusive. The NE is continuous with the endoplasmic reticulum (ER) and recent evidence suggests that lipids produced in the ER are harnessed to remodel nuclear membranes. In this review, we examine new roles for lipid species made proximally within the ER and locally at the NE to control NE dynamics. We further explore how the biosynthesis of lipids coordinates NE remodeling to ensure genome protection.

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References

Campbell J, Lorenz A, Witkin K, Hays T, Loidl J, Cohen-Fix O . Yeast nuclear envelope subdomains with distinct abilities to resist membrane expansion. Mol Biol Cell. 2006; 17(4):1768-78. PMC: 1415286. DOI: 10.1091/mbc.e05-09-0839. View

Luithle N, de Bos J, Hovius R, Maslennikova D, Lewis R, Ungricht R . Torsin ATPases influence chromatin interaction of the Torsin regulator LAP1. Elife. 2020; 9. PMC: 7773337. DOI: 10.7554/eLife.63614. View

Earle A, Kirby T, Fedorchak G, Isermann P, Patel J, Iruvanti S . Mutant lamins cause nuclear envelope rupture and DNA damage in skeletal muscle cells. Nat Mater. 2019; 19(4):464-473. PMC: 7102937. DOI: 10.1038/s41563-019-0563-5. View

Schoen I, Aires L, Ries J, Vogel V . Nanoscale invaginations of the nuclear envelope: Shedding new light on wormholes with elusive function. Nucleus. 2017; 8(5):506-514. PMC: 5703262. DOI: 10.1080/19491034.2017.1337621. View

Champion L, Pawar S, Luithle N, Ungricht R, Kutay U . Dissociation of membrane-chromatin contacts is required for proper chromosome segregation in mitosis. Mol Biol Cell. 2018; 30(4):427-440. PMC: 6594442. DOI: 10.1091/mbc.E18-10-0609. View

Lomakin A, Cattin C, Cuvelier D, Alraies Z, Molina M, Nader G . The nucleus acts as a ruler tailoring cell responses to spatial constraints. Science. 2020; 370(6514). PMC: 8059074. DOI: 10.1126/science.aba2894. View

Schroeder L, Barentine A, Merta H, Schweighofer S, Zhang Y, Baddeley D . Dynamic nanoscale morphology of the ER surveyed by STED microscopy. J Cell Biol. 2018; 218(1):83-96. PMC: 6314542. DOI: 10.1083/jcb.201809107. View

Walters A, Amoateng K, Wang R, Chen J, McDermott G, Larabell C . Nuclear envelope expansion in budding yeast is independent of cell growth and does not determine nuclear volume. Mol Biol Cell. 2018; 30(1):131-145. PMC: 6337908. DOI: 10.1091/mbc.E18-04-0204. View

Schlaitz A, Thompson J, Wong C, Yates 3rd J, Heald R . REEP3/4 ensure endoplasmic reticulum clearance from metaphase chromatin and proper nuclear envelope architecture. Dev Cell. 2013; 26(3):315-23. PMC: 3745822. DOI: 10.1016/j.devcel.2013.06.016. View

10.

Kim Y, Gentry M, Harris T, Wiley S, Lawrence Jr J, Dixon J . A conserved phosphatase cascade that regulates nuclear membrane biogenesis. Proc Natl Acad Sci U S A. 2007; 104(16):6596-601. PMC: 1871831. DOI: 10.1073/pnas.0702099104. View

11.

Bahmanyar S, Schlieker C . Lipid and protein dynamics that shape nuclear envelope identity. Mol Biol Cell. 2020; 31(13):1315-1323. PMC: 7353140. DOI: 10.1091/mbc.E18-10-0636. View

12.

Tsai P, Zhao C, Turner E, Schlieker C . The Lamin B receptor is essential for cholesterol synthesis and perturbed by disease-causing mutations. Elife. 2016; 5. PMC: 4951196. DOI: 10.7554/eLife.16011. View

13.

Barelli H, Antonny B . Lipid unsaturation and organelle dynamics. Curr Opin Cell Biol. 2016; 41:25-32. DOI: 10.1016/j.ceb.2016.03.012. View

14.

Boroda S, Takkellapati S, Lawrence R, Entwisle S, Pearson J, Granade M . The phosphatidic acid-binding, polybasic domain is responsible for the differences in the phosphoregulation of lipins 1 and 3. J Biol Chem. 2017; 292(50):20481-20493. PMC: 5733587. DOI: 10.1074/jbc.M117.786574. View

15.

Siniossoglou S . Phospholipid metabolism and nuclear function: roles of the lipin family of phosphatidic acid phosphatases. Biochim Biophys Acta. 2012; 1831(3):575-81. DOI: 10.1016/j.bbalip.2012.09.014. View

16.

Anderson D, Hetzer M . Nuclear envelope formation by chromatin-mediated reorganization of the endoplasmic reticulum. Nat Cell Biol. 2007; 9(10):1160-6. DOI: 10.1038/ncb1636. View

17.

Hatch E . Nuclear envelope rupture: little holes, big openings. Curr Opin Cell Biol. 2018; 52:66-72. PMC: 5988944. DOI: 10.1016/j.ceb.2018.02.001. View

18.

Zegarlinska J, Piascik M, Sikorski A, Czogalla A . Phosphatidic acid - a simple phospholipid with multiple faces. Acta Biochim Pol. 2018; 65(2):163-171. DOI: 10.18388/abp.2018_2592. View

19.

Gorjanacz M, Mattaj I . Lipin is required for efficient breakdown of the nuclear envelope in Caenorhabditis elegans. J Cell Sci. 2009; 122(Pt 12):1963-9. DOI: 10.1242/jcs.044750. View

20.

Barbosa A, Lim K, Mari M, Edgar J, Gal L, Sterk P . Compartmentalized Synthesis of Triacylglycerol at the Inner Nuclear Membrane Regulates Nuclear Organization. Dev Cell. 2019; 50(6):755-766.e6. PMC: 6859503. DOI: 10.1016/j.devcel.2019.07.009. View