Breaching the Nuclear Envelope in Development and Disease

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 2014 Apr 23

PMID 24751535

Citations 71

Authors

Emily Hatch

Martin Hetzer

Affiliations

Soon will be listed here.

Abstract

In eukaryotic cells the nuclear genome is enclosed by the nuclear envelope (NE). In metazoans, the NE breaks down in mitosis and it has been assumed that the physical barrier separating nucleoplasm and cytoplasm remains intact during the rest of the cell cycle and cell differentiation. However, recent studies suggest that nonmitotic NE remodeling plays a critical role in development, virus infection, laminopathies, and cancer. Although the mechanisms underlying these NE restructuring events are currently being defined, one common theme is activation of protein kinase C family members in the interphase nucleus to disrupt the nuclear lamina, demonstrating the importance of the lamina in maintaining nuclear integrity.

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References

Wente S, Rout M . The nuclear pore complex and nuclear transport. Cold Spring Harb Perspect Biol. 2010; 2(10):a000562. PMC: 2944363. DOI: 10.1101/cshperspect.a000562. View

Lenart P, Ellenberg J . Nuclear envelope dynamics in oocytes: from germinal vesicle breakdown to mitosis. Curr Opin Cell Biol. 2003; 15(1):88-95. DOI: 10.1016/s0955-0674(02)00011-x. View

Milbradt J, Webel R, Auerochs S, Sticht H, Marschall M . Novel mode of phosphorylation-triggered reorganization of the nuclear lamina during nuclear egress of human cytomegalovirus. J Biol Chem. 2010; 285(18):13979-89. PMC: 2859560. DOI: 10.1074/jbc.M109.063628. View

Marschall M, Feichtinger S, Milbradt J . Regulatory roles of protein kinases in cytomegalovirus replication. Adv Virus Res. 2011; 80:69-101. DOI: 10.1016/B978-0-12-385987-7.00004-X. View

Devos D, Dokudovskaya S, Williams R, Alber F, Eswar N, Chait B . Simple fold composition and modular architecture of the nuclear pore complex. Proc Natl Acad Sci U S A. 2006; 103(7):2172-7. PMC: 1413685. DOI: 10.1073/pnas.0506345103. View

Doucet C, Talamas J, Hetzer M . Cell cycle-dependent differences in nuclear pore complex assembly in metazoa. Cell. 2010; 141(6):1030-41. PMC: 2887351. DOI: 10.1016/j.cell.2010.04.036. View

Mor A, Suliman S, Ben-Yishay R, Yunger S, Brody Y, Shav-Tal Y . Dynamics of single mRNP nucleocytoplasmic transport and export through the nuclear pore in living cells. Nat Cell Biol. 2010; 12(6):543-52. DOI: 10.1038/ncb2056. View

Lu L, Ladinsky M, Kirchhausen T . Formation of the postmitotic nuclear envelope from extended ER cisternae precedes nuclear pore assembly. J Cell Biol. 2011; 194(3):425-40. PMC: 3153650. DOI: 10.1083/jcb.201012063. View

Beaudouin J, Gerlich D, Daigle N, Eils R, Ellenberg J . Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina. Cell. 2002; 108(1):83-96. DOI: 10.1016/s0092-8674(01)00627-4. View

10.

Hochstrasser M, Sedat J . Three-dimensional organization of Drosophila melanogaster interphase nuclei. II. Chromosome spatial organization and gene regulation. J Cell Biol. 1987; 104(6):1471-83. PMC: 2114521. DOI: 10.1083/jcb.104.6.1471. View

11.

Kiseleva E, GOLDBERG M, ALLEN T, Akey C . Active nuclear pore complexes in Chironomus: visualization of transporter configurations related to mRNP export. J Cell Sci. 1998; 111 ( Pt 2):223-36. DOI: 10.1242/jcs.111.2.223. View

12.

Casey A, Dawson T, Chen J, Friederichs J, Jaspersen S, Wente S . Integrity and function of the Saccharomyces cerevisiae spindle pole body depends on connections between the membrane proteins Ndc1, Rtn1, and Yop1. Genetics. 2012; 192(2):441-55. PMC: 3454875. DOI: 10.1534/genetics.112.141465. View

13.

Cross T, Griffiths G, Deacon E, Sallis R, Gough M, Watters D . PKC-delta is an apoptotic lamin kinase. Oncogene. 2000; 19(19):2331-7. DOI: 10.1038/sj.onc.1203555. View

14.

Oliva H, Valle A, Flores L, Rivas M . Intranuclear mitochondriae in Hodgkin's disease. Virchows Arch B Cell Pathol. 1973; 12(2):189-94. DOI: 10.1007/BF02893997. View

15.

Grunwald D, Singer R, Rout M . Nuclear export dynamics of RNA-protein complexes. Nature. 2011; 475(7356):333-41. PMC: 3154952. DOI: 10.1038/nature10318. 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.

Dechat T, Adam S, Taimen P, Shimi T, Goldman R . Nuclear lamins. Cold Spring Harb Perspect Biol. 2010; 2(11):a000547. PMC: 2964183. DOI: 10.1101/cshperspect.a000547. View

18.

Hanson P, Whiteheart S . AAA+ proteins: have engine, will work. Nat Rev Mol Cell Biol. 2005; 6(7):519-29. DOI: 10.1038/nrm1684. View

19.

HADEK R, Swift H . Nuclear extrusion and intracisternal inclusions in the rabbit blastocyst. J Cell Biol. 1962; 13:445-51. PMC: 2106075. DOI: 10.1083/jcb.13.3.445. View

20.

Goss V, Hocevar B, Thompson L, Stratton C, Burns D, Fields A . Identification of nuclear beta II protein kinase C as a mitotic lamin kinase. J Biol Chem. 1994; 269(29):19074-80. View