2,243
Views
2
CrossRef citations to date
0
Altmetric
Review

Nuclear envelope budding and its cellular functions

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Article: 2178184 | Received 13 Oct 2022, Accepted 03 Feb 2023, Published online: 22 Feb 2023

References

  • Keuenhof KS, Larsson Berglund L, Malmgren Hill S, et al. Large organellar changes occur during mild heat shock in yeast. J Cell Sci. 2022;135(5):1–19.
  • Austin CR, Braden AWH. Observations on nuclear size and form in living rat and mouse eggs. Exp Cell Res. 1955;8(1):163–172.
  • Lambert RA. Comparative studies upon cancer cells and normal cells: II. the character of growth in vitro with special reference to cell division. J Exp Med. 1913;17(5):499–510.
  • Jorgensen P, Edgington NP, Schneider BL, et al. The Size of the Nucleus Increases as Yeast Cells Grow. Mol Biol Cell. 2007 Sep;18(9):3523–3532.
  • Wilson EB. The Cell in Development and Heredity. 3rd ed. New York: The Macmillan Company; 1925.
  • Zidovska A. The rich inner life of the cell nucleus: dynamic organization, active flows, and emergent rheology. Biophys Rev. 2020 Oct;12(5):1093–1106.
  • Beck M, Hurt E. The nuclear pore complex: understanding its function through structural insight. Nat Rev Mol Cell Biol. 2017 Feb;18(2):73–89.
  • Lusk CP, King MC. The nucleus: keeping it together by keeping it apart. Curr Opin Cell Biol. 2017 Feb;44(1):44–50.
  • Lammerding J. Comprehensive Physiology. In: Terjung R, editor. Mechanics of the Nucleus. Wiley; 2011. p. 783–807. DOI:10.1002/cphy.c100038
  • Szollosi D. Extrusion of nucleoli from pronuclei of the rat. J Cell Biol. 1965 Jun;25(3):545–562.
  • Szollosi MS, Szollosi D. ‘Blebbing’ of the nuclear envelope of mouse zygotes, early embryos and hybrid cells. J Cell Sci. 1988 Oct;91(2):257–267.
  • Hochstrasser M, Sedat JW. Three-dimensional organization of Drosophila melanogaster interphase nuclei. II. Chromosome spatial organization and gene regulation. J Cell Biol. 1987 Jun;104(6):1471–1483.
  • LaMassa N, Arenas-Mena C, Phillips GR. Electron microscopic characterization of nuclear egress in the sea urchin gastrula. J Morphol. 2018 May;279(5):609–615.
  • Aldrich HC, Vasil IK. Ultrastructure of the postmeiotic nuclear envelope in microspores of Podocarpus macrophyllus. J Ultrastruct Res. 1970 Aug;32(3–4):307–315.
  • Gullvåg BM. Release of Nuclear Material During the Development of Lycopodium Annotinum L. Spores. Grana. 1970 Jan;10(1):31–34.
  • Afzelius BA. The nucleus of Noctiluca scintillans. J Cell Biol. 1963 Oct;19(1):229–238.
  • Elston RN, Stenkvist B. Quantitative estimation of nuclear buds and micronuclei in bovine cells transformed by Rous sarcoma and SV 40 viruses. Zeitschrift für Zellforschung und Mikroskopische Anatomie. 1965;68(4):543–549.
  • Dickinson HG, Bell PR. Nucleocytoplasmic interaction at the nuclear envelope in post meiotic microspores of Pinus banksiana. J Ultrastruct Res. 1970 Nov;33(3–4):356–359.
  • Mepham RH, Lane GR. Observations on the fine structure of developing microspores of Tradescantia bracteata. Protoplasma. 1970;70(1):1–20.
  • Dickinson HG. Nucleo-cytoplasmic interaction following meiosis in the young microspores of Lilium longiflorum; events at the nuclear envelope. Grana. 1971;11(2):117–127.
  • Gay H. Nucleo-cytoplasmic relations in salivary-gland cells of Drosophila. Proceedings of the National Academy of Sciences. Jun 1955;41(6):370–375
  • Romanauska A, Köhler A. The Inner Nuclear Membrane Is a Metabolically Active Territory that Generates Nuclear Lipid Droplets. Cell. 2018 Jul;174(3):700–715.e18.
  • Longwell AC, Yerganian G. Some Observations on Nuclear Budding and Nuclear Extrusions in a Chinese Hamster Cell Culture. Jnci. 1965 Jan;34(1):53–69.
  • Goodchild RE, Kim CE, Dauer WT. Loss of the dystonia-associated protein torsinA selectively disrupts the neuronal nuclear envelope. Neuron. 2005;48(6):923–932.
  • Tanabe LM, Liang CC, Dauer WT. Neuronal Nuclear Membrane Budding Occurs during a Developmental Window Modulated by Torsin Paralogs. Cell Rep. 2016;16(12):3322–3333.
  • Tanabe LM, Martin C, Dauer WT. Genetic background modulates the phenotype of a mouse model of dyt1 dystonia. PLoS One. 2012;7(2):1–9.
  • Panagaki D, Croft JT, Keuenhof K, et al. Nuclear envelope budding is a response to cellular stress. 2021;118(30). DOI:10.1073/pnas.2020997118
  • Speese SD, Ashley J, Jokhi V, et al. Nuclear Envelope Budding Enables Large Ribonucleoprotein Particle Export during Synaptic Wnt Signaling. Cell. 2012 May;149(4):832–846.
  • Ding B, Mirza AM, Ashley J, et al. “Nuclear Export Through Nuclear Envelope Remodeling in Saccharomyces cerevisiae. bioRxiv. 2017;224055.
  • Chandra S, Mannino P, Thaller D, et al. Atg39 selectively captures inner nuclear membrane into lumenal vesicles for delivery to the autophagosome. J Cell Bio. 2021 Dec;220(12):2021. 02.22.432332.
  • Thaller DJ, Patrick Lusk C. Fantastic nuclear envelope herniations and where to find them. Biochem Soc Trans. 2018 Aug;46(4):877–889.
  • Hadek R, Swift H. Nuclear extrusion and intracisternal inclusions in the rabbit blastocyst. J Cell Biol. 1962 Jun;13(3):445–451.
  • Gay H. Chromosome-nuclear membrane-cytoplasmic interrelations in Drosophila. J Biophys Biochem Cytol. 1956 Jul;2(4):407–414.
  • Verboon JM, Nakamura M, Davidson KA, et al. Drosophila Wash and the Wash regulatory complex function in nuclear envelope budding. J Cell Sci. 2020 Jan;130(13):jcs243576.
  • Rempel IL, Crane M, Thaller DJ, et al. Age-dependent deterioration of nuclear pore assembly in mitotic cells decreases transport dynamics. Elife. 2019Jun;8:1–26.
  • Feldherr CM. The nuclear annuli as pathways for nucleocytoplasmic exchanges. J Cell Biol. 1962 Jul;14(1):65–72.
  • Richardson WD, Mills AD, Dilworth SM, et al. Nuclear protein migration involves two steps: rapid binding at the nuclear envelope followed by slower translocation through nuclear pores. Cell. 1988 Mar;52(5):655–664.
  • Dworetzky SI, Feldherr CM. Translocation of RNA-coated gold particles through the nuclear pores of oocytes. J Cell Biol. 1988;106(3):575–584.
  • Görlich D, Kutay U. Transport Between the Cell Nucleus and the Cytoplasm. Annu Rev Cell Dev Biol. 1999 Nov;15(1):607–660.
  • Zetka M, Paouneskou D, Jantsch V. ‘The nuclear envelope, a meiotic jack-of-all-trades,’. Curr Opin Cell Biol. 2020;64:34–42.
  • de Magistris P, Antonin W. The Dynamic Nature of the Nuclear Envelope. Curr Biol. 2018 Apr;28(8):R487–R497.
  • Knockenhauer KE, Schwartz TU. The Nuclear Pore Complex as a Flexible and Dynamic Gate. Cell. 2016;164(6):1162–1171.
  • Kabachinski G, Schwartz TU. The nuclear pore complex - Structure and function at a glance. J Cell Sci. 2015;128(3):423–429.
  • Lin DH, Hoelz A. The structure of the nuclear pore complex (An Update). Annu Rev Biochem. 2019;88:725–783.
  • Reichelt R, Holzenburg A, Buhle EL, et al. Correlation between structure and mass distribution of the nuclear pore complex and of distinct pore complex components. J Cell Biol. 1990;110(4):883–894.
  • Yang Q, Rout MP, Akey CW. Three-dimensional architecture of the isolated yeast nuclear pore complex: functional and evolutionary implications. Mol Cell. 1998;1(2):223–234.
  • Rout MP, Aitchison JD, Suprapto A, et al. The yeast nuclear pore complex: composition, architecture, transport mechanism. J Cell Biol. 2000;148(4):635–651.
  • Tamura K, Fukao Y, Iwamoto M, et al. Identification and Characterization of Nuclear Pore Complex Components in Arabidopsis thaliana. Plant Cell. 2011 Jan;22(12):4084–4097.
  • DeGrasse JA, Dubois KN, Devos D, et al. Evidence for a shared nuclear pore complex architecture that is conserved from the last common eukaryotic ancestor. Molecular and Cellular Proteomics. 2009;8(9):2119–2130.
  • Cronshaw JM, Krutchinsky AN, Zhang W, et al. Proteomic analysis of the mammalian nuclear pore complex. J Cell Biol. 2002;158(5):915–927.
  • Hampoelz B, Andres-Pons A, Kastritis P, et al. Structure and Assembly of the Nuclear Pore Complex. Annu Rev Biophys. 2019;48:515–536.
  • Akey CW, Singh D, Ouch C, et al. Comprehensive structure and functional adaptations of the yeast nuclear pore complex. Cell. 2022;185(2):361–378.e25.
  • Watson ML. Further Observations on the Nuclear Envelope of the Animal Cell. J Biophys Biochem Cytol. 1959 Oct;6(2):147–156.
  • Naim B, Zbaida D, Dagan S, et al. Cargo surface hydrophobicity is sufficient to overcome the nuclear pore complex selectivity barrier. EMBO J. 2009;28(18):2697–2705.
  • Frey S, Rees R, Schünemann J, et al. Surface Properties Determining Passage Rates of Proteins through Nuclear Pores. Cell. 2018;174(1):202–217.e9.
  • Wang R, Brattain MG. The maximal size of protein to diffuse through the nuclear pore is larger than 60 kDa. FEBS Lett. 2007;581(17):3164–3170.
  • Fradkin LG, Budnik V. This bud’s for you: mechanisms of cellular nucleocytoplasmic trafficking via nuclear envelope budding. Curr Opin Cell Biol. 2016 Aug;41(3):125–131.
  • Parchure A, Munson M, Budnik V. Getting mRNA-Containing Ribonucleoprotein Granules Out of a Nuclear Back Door. Neuron. 2017 Nov;96(3):604–615.
  • Li Y, Hassinger L, Thomson L, et al. Lamin Mutations Accelerate Aging via Defective Export of Mitochondrial mRNAs through Nuclear Envelope Budding. Curr Biol. 2016;26(15):2052–2059.
  • Jokhi V, Ashley J, Nunnari J, et al. Torsin Mediates Primary Envelopment of Large Ribonucleoprotein Granules at the Nuclear Envelope. Cell Rep. 2013;3(4):988–995.
  • Cabrita MA, Renart LI, Lau R, et al. Intrinsically disordered SRC-3/AIB1 protein undergoes homeostatic nuclear extrusion by nuclear budding while ectopic expression induces nucleophagy. Cells. 2019;8(10):Oct.
  • Otto FB, Thumm M. Mechanistic dissection of macro- and micronucleophagy. Autophagy. 2021 Mar;17(3):626–639.
  • Hagen C, Dent KC, Zeev-Ben-Mordehai T, et al. Structural Basis of Vesicle Formation at the Inner Nuclear Membrane. Cell. 2015 Dec;163(7):1692–1701.
  • Lorenz M, Vollmer B, Unsay JD, et al. A single herpesvirus protein can mediate vesicle formation in the nuclear envelope. J Biol Chem. 2015;290(11):6962–6974.
  • Liu Z, Kato A, Oyama M, et al. Role of Host Cell p32 in Herpes Simplex Virus 1 De-Envelopment during Viral Nuclear Egress. J Virol. 2015;89(17):8982–8998.
  • Roller RJ, Bjerke SL, Haugo AC, et al. 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):3921–3934.
  • Smith AE, Helenius A. How Viruses Enter Animal Cells. Sci (1979). 2004;304(5668):237–242.
  • Molenberghs F, Bogers JJ, de Vos WH. Confined no more: viral mechanisms of nuclear entry and egress. Int J Biochem Cell Biol. 2020Dec;129:105875.
  • de Castro IJ, Lusic M. Navigating through the nucleus with a virus. Curr Opin Genet Dev. 2019;55:100–105.
  • Lucifora J, Delphin M. Current knowledge on Hepatitis Delta Virus replication. Antiviral Res. 2020;179:104812.
  • Lucic B, de Castro IJ, Lusic M. Viruses in the Nucleus. Cold Spring Harb Perspect Biol. 2021 Aug;13(8):a039446.
  • Mäntylä E, Niskanen EA, Ihalainen TO, et al. Reorganization of Nuclear Pore Complexes and the Lamina in Late-Stage Parvovirus Infection. J Virol. 2015;89(22):11706–11710.
  • Giorda KM, Raghava S, Hebert DN. The Simian Virus 40 Late Viral Protein VP4 Disrupts the Nuclear Envelope for Viral Release. J Virol. 2012;86(6):3180–3192.
  • Raghava S, Giorda KM, Romano FB, et al. SV40 late protein VP4 forms toroidal pores to disrupt membranes for viral release. Biochemistry. 2013;52(22):3939–3948.
  • Davison AJ, Eberle R, Ehlers B, et al. The order Herpesvirales. Arch Virol. 2009;154(1):171–177.
  • Marschall M, Häge S, Conrad M, et al. Nuclear Egress Complexes of HCMV and Other Herpesviruses: solving the Puzzle of Sequence Coevolution, Conserved Structures and Subfamily-Spanning Binding Properties. Viruses. 2020;12(6): 683.
  • Roller RJ, Baines JD. Herpesvirus Nuclear Egress. In: Osterrieder K, editor. Cell Biology of Herpes Viruses. Vol. 223. Springer; 2017. p. 143–169.
  • Ahmad I, Wilson DW. HSV-1 Cytoplasmic Envelopment and Egress. Int J Mol Sci. 2020 Aug;21(17):5969.
  • Shiba C, Daikoku T, Goshima F, et al. The UL34 gene product of herpes simplex virus type 2 is a tail-anchored type II membrane protein that is significant for virus envelopment. J Gen Virol. 2000;81(10):2397–2405.
  • Chang YE, Roizman B. The product of the UL31 gene of herpes simplex virus 1 is a nuclear phosphoprotein which partitions with the nuclear matrix. J Virol. 1993;67(11):6348–6356.
  • Reynolds AE, Wills EG, Roller RJ, et al. 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 Sep;76(17):8939–8952.
  • Bigalke JM, Heldwein EE. The Great (Nuclear) Escape: new Insights into the Role of the Nuclear Egress Complex of Herpesviruses. J Virol. 2015;89(18):9150–9153.
  • Wong X, Melendez-Perez AJ, Reddy KL. The Nuclear Lamina. Cold Spring Harb Perspect Biol. 2022 Feb;14(2):a040113.
  • Reynolds AE, Liang L, Baines JD. Conformational Changes in the Nuclear Lamina Induced by Herpes Simplex Virus Type 1 Require Genes UL31 and UL34. J Virol. 2004 Jun;78(11):5564–5575.
  • Park R, Baines JD. Herpes Simplex Virus Type 1 Infection Induces Activation and Recruitment of Protein Kinase C to the Nuclear Membrane and Increased Phosphorylation of Lamin B. J Virol. 2006;80(1):494–504.
  • Morris JB, Hofemeister H, O’Hare P. Herpes Simplex Virus Infection Induces Phosphorylation and Delocalization of Emerin, a Key Inner Nuclear Membrane Protein. J Virol. 2007;81(9):4429–4437.
  • Mou F, Forest T, Baines JD. US3 of Herpes Simplex Virus Type 1 Encodes a Promiscuous Protein Kinase That Phosphorylates and Alters Localization of Lamin A/C in Infected Cells. J Virol. 2007;81(12):6459–6470.
  • Bjerke SL, Roller RJ. Roles for herpes simplex virus type 1 UL34 and US3 proteins in disrupting the nuclear lamina during herpes simplex virus type 1 egress. Virology. 2006 Apr;347(2):261–276.
  • Hamirally S, Kamil JP, Ndassa-Colday YM, et al. Viral mimicry of Cdc2/cyclin-dependent kinase 1 mediates disruption of nuclear lamina during human cytomegalovirus nuclear egress. PLoS Pathog. 2009;5(1). DOI:10.1371/journal.ppat.1000275
  • Chang YE, van Sant C, Krug PW, et al. The null mutant of the UL31 gene of herpes simplex virus 1: construction and phenotype in infected cells. J Virol. 1997 Nov;71(11):8307–8315.
  • Klupp BG, Granzow H, Mettenleiter TC. Primary Envelopment of Pseudorabies Virus at the Nuclear Membrane Requires the UL34 Gene Product. J Virol. 2000;74(21):10063–10073.
  • Roller RJ, Zhou Y, Schnetzer R, et al. Herpes Simplex Virus Type 1 UL34 Gene Product Is Required for Viral Envelopment. J Virol. 2000 Jan;74(1):117–129.
  • Arii J, Watanabe M, Maeda F, et al. ESCRT-III mediates budding across the inner nuclear membrane and regulates its integrity. Nat Commun. 2018;9(1).
  • Wagenaar F, Pol JMA, Peeters B, et al. The US3-encoded protein kinase from pseudorabies virus affects egress of virions from the nucleus. J Gen Virol. 1995;76(7):1851–1859.
  • Liu Z, Kato A, Shindo K, et al. Herpes Simplex Virus 1 UL47 Interacts with Viral Nuclear Egress Factors UL31, UL34, and Us3 and Regulates Viral Nuclear Egress. J Virol. 2014 May;88(9):4657–4667.
  • Sigrist SJ, Thiel PR, Reiff DF, et al. Postsynaptic translation affects the efficacy and morphology of neuromuscular junctions. Nature. 2000 Jun;405(6790):1062–1065.
  • Linardopoulou EV, Parghi SS, Friedman C, et al. Human subtelomeric WASH genes encode a new subclass of the WASP family. PLoS Genet. 2007;3(12):2477–2485.
  • Rose A, Schlieker C. Alternative nuclear transport for cellular protein quality control. Trends Cell Biol. 2012 Oct;22(10):509–514.
  • Ciechanover A. The ubiquitin-proteasome pathway: on protein death and cell life. EMBO J. 1998 Dec;17(24):7151–7160.
  • Chen B, Retzlaff M, Roos T, et al., “Cellular Strategies of Protein Quality Control”, doi: 10.1101/cshperspect.a004374.
  • Escusa-Toret S, Vonk WIM, Frydman J. Spatial sequestration of misfolded proteins by a dynamic chaperone pathway enhances cellular fitness during stress. Nat Cell Biol. 2013 Oct;15(10):1231–1243.
  • Hill SM, Hanzén S, Nyström T. Restricted access: spatial sequestration of damaged proteins during stress and aging. EMBO Rep. 2017;18(3):377–391.
  • Sontag EM, Samant RS, Frydman J. Mechanisms and Functions of Spatial Protein Quality Control. Annu Rev Biochem. 2017 Jun;86(1):97–122.
  • Schneider KL, Nyström T, Widlund PO. Studying Spatial Protein Quality Control, Proteopathies, and Aging Using Different Model Misfolding Proteins in S. Cerevisiae. Front Mol Neurosci. 2018;11:1–13.
  • Kumar A, Mathew V, Stirling PC. Nuclear protein quality control in yeast: the latest INQuiries. J Biol Chem. 2022;298(8):102199.
  • Mochida K, Otani T, Katsuma Y, et al. Atg39 links and deforms the outer and inner nuclear membranes in selective autophagy of the nucleus. J Cell Biol. 2022Feb;221(2).
  • Mannino PJ, Lusk CP. Quality control mechanisms that protect nuclear envelope identity and function. J Cell Biol. 2022 Sep;221(9):1–13.
  • Mochida K, Oikawa Y, Kimura Y, et al. Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus. Nature. 2015;522(7556):359–362.
  • Webster BM, Colombi P, Jäger J, et al. Surveillance of nuclear pore complex assembly by ESCRT-III/Vps4. Cell. 2014;159(2):388–401.
  • Mizuno T, Irie K. Msn2/4 transcription factors positively regulate expression of Atg39 ER-phagy receptor. Sci Rep. 2021;11(1):1–12.
  • King GA, Goodman JS, Schick JG, et al. Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast. Elife. 2019Aug;8:1–32.
  • Denoth Lippuner A, Julou T, Barral Y. Budding yeast as a model organism to study the effects of age. FEMS Microbiol Rev. 2014 Mar;38(2):300–325.
  • Lusk CP, Colombi P. Toward a consensus on the mechanism of nuclear pore complex inheritance. Nucleus. 2014 Mar;5(2):97–102.
  • Makio T, Lapetina DL, Wozniak RW. Inheritance of yeast nuclear pore complexes requires the Nsp1p subcomplex. J Cell Biol. 2013 Oct;203(2):187–196.
  • Colombi P, Webster BM, Fröhlich F, et al. The transmission of nuclear pore complexes to daughter cells requires a cytoplasmic pool of Nsp1. J Cell Biol. 2013 Oct;203(2):215–232.
  • Bucci M, Wente SR. A Novel Fluorescence-based Genetic Strategy Identifies Mutants of Saccharomyces cerevisiae Defective for Nuclear Pore Complex Assembly. Mol Biol Cell. 1998 Sep;9(9):2439–2461.
  • Siniossoglou S, Wimmer C, Rieger M, et al. A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores. Cell. 1996;84(2):265–275.
  • Onischenko E, Tang JH, Andersen KR, et al. Natively Unfolded FG Repeats Stabilize the Structure of the Nuclear Pore Complex. Cell. 2017;171(4):904–917.e19.
  • Gigliotti S, Callaini G, Andone S, et al. Nup154, a new Drosophila gene essential for male and female gametogenesis is related to the Nup155 vertebrate nucleoporin gene. J Cell Biol. 1998;142(5):1195–1207.
  • Schneiter R, Hitomi M, Ivessa AS, et al. A yeast acetyl coenzyme A carboxylase mutant links very-long-chain fatty acid synthesis to the structure and function of the nuclear membrane-pore complex. Mol Cell Biol. 1996 Dec;16(12):7161–7172.
  • Wente SR, Blobel G. A temperature-sensitive NUP116 null mutant forms a nuclear envelope seal over the yeast nuclear pore complex thereby blocking nucleocytoplasmic traffic. J Cell Biol. 1993 Oct;123(2):275–284.
  • Webster BM, Thaller DJ, Jäger J, et al. Chm7 and Heh1 collaborate to link nuclear pore complex quality control with nuclear envelope sealing. EMBO J. 2016;35(22):2447–2467.
  • Fernandez-Martinez J, Rout MP. Nuclear pore complex biogenesis. Curr Opin Cell Biol. 2009;21(4):603–612.
  • Allegretti M, Zimmerli CE, Rantos V, et al. In-cell architecture of the nuclear pore and snapshots of its turnover. Nature. 2020 Oct;586(7831):796–800.
  • Turner EM, Brown RSH, Laudermilch E, et al. The Torsin Activator LULL1 Is Required for Efficient Growth of Herpes Simplex Virus 1. J Virol. 2015;89(16):8444–8452.
  • Maric M, Shao J, Ryan RJ, et al. A Functional Role for TorsinA in Herpes Simplex Virus 1 Nuclear Egress. J Virol. 2011;85(19):9667–9679.
  • Laudermilch E, Tsai PL, Graham M, et al. Dissecting Torsin/cofactor function at the nuclear envelope: a genetic study. Mol Biol Cell. 2016;27(25):3964–3971.
  • Rampello AJ, Laudermilch E, Vishnoi N, et al. Torsin ATPase deficiency leads to defects in nuclear pore biogenesis and sequestration of MLF2. J Cell Biol. 2020;6:219.
  • Pappas SS, Liang C-C, Kim S, et al. TorsinA dysfunction causes persistent neuronal nuclear pore defects. Hum Mol Genet. 2018 Feb;27(3):407–420.
  • von Appen A, LaJoie D, Johnson IE, et al. LEM2 phase separation promotes ESCRT-mediated nuclear envelope reformation. Nature. 2020;582(7810):115–118.
  • Koch BA, Staley E, Jin H, et al. The ESCRT-III complex is required for nuclear pore complex sequestration and regulates gamete replicative lifespan in budding yeast meiosis. Nucleus. 2020;11(1):219–236.
  • Thaller DJ, Tong D, Marklew CJ, et al. Direct binding of ESCRT protein Chm7 to phosphatidic acid-rich membranes at nuclear envelope herniations. J Cell Biol. 2021;3:220.
  • Faleiro L, Lazebnik Y. Caspases disrupt the nuclear-cytoplasmic barrier. J Cell Biol. 2000;151(5):951–959.
  • Ferrando-May E, Cordes V, Biller-Ckovric I, et al. Caspases mediate nucleoporin cleavage, but not early redistribution of nuclear transport factors and modulation of nuclear permeability in apoptosis. Cell Death Differ. 2001;8(5):495–505.
  • Gomez GN, Abrar F, Dodhia MP, et al. SARS coronavirus protein nsp1 disrupts localization of Nup93 from the nuclear pore complex. Biochem Cell Biol. 2019 Dec;97(6):758–766.
  • Patre M, Tabbert A, Hermann D, et al. Caspases target only two architectural components within the core structure of the nuclear pore complex. J Biol Chem. 2006;281(2):1296–1304.
  • Yarbrough ML, Mata MA, Sakthivel R, et al. Viral Subversion of Nucleocytoplasmic Trafficking. Traffic. 2014 Feb;15(2):127–140.
  • Liu J, Hetzer MW. Nuclear pore complex maintenance and implications for age-related diseases. Trends Cell Biol. 2022 Mar;32(3):216–227.
  • Savas JN, Toyama BH, Xu T, et al. Extremely long-lived nuclear pore proteins in the rat brain. Sci (1979). 2012;335(6071):942.
  • Lee CW, Wilfling F, Ronchi P, et al. Selective autophagy degrades nuclear pore complexes. Nat Cell Biol. 2020;22(2):159–166.
  • Shcheprova Z, Baldi S, Frei SB, et al. A mechanism for asymmetric segregation of age during yeast budding. Nature. 2008;454(7205):728–734.
  • Toyama BH, Savas JN, Park SK, et al. Identification of Long-Lived Proteins Reveals Exceptional Stability of Essential Cellular Structures. Cell. 2013 Aug;154(5):971–982.
  • D’Angelo MA, Raices M, Panowski SH, et al. Age-Dependent Deterioration of Nuclear Pore Complexes Causes a Loss of Nuclear Integrity in Postmitotic Cells. Cell. 2009 Jan;136(2):284–295.
  • Rempel IL, Steen A, Veenhoff LM. Poor old pores—The challenge of making and maintaining nuclear pore complexes in aging. FEBS J. 2020 Mar;287(6):1058–1075.
  • Gross AS, Graef M. Stress eating: autophagy targets nuclear pore complexes. J Cell Biol. 2020 Jul;219(7):7–8.
  • Sakuma S, D’Angelo MA. The roles of the nuclear pore complex in cellular dysfunction, aging and disease. Semin Cell Dev Biol. 2017 Aug;68(10):72–84.
  • Bussolati G, Maletta F, Asioli S, et al. Advances in Experimental Medicine and Biology. In: To Be or Not to Be in a Good Shape’: diagnostic and Clinical Value of Nuclear Shape Irregularities in Thyroid and Breast Cancer. Vol. 773. New York, NY: Springer;2014. p.101–121.
  • B Ding, Tang Y, Ma S, et al. Disease modeling with human neurons reveals lmnb1 dysregulation underlying dyt1 dystonia. J Neurosci. 2021;41(9):2024–2038.
  • Li N, Lagier-Tourenne C. Nuclear pores: the gate to neurodegeneration. Nat Neurosci. 2018 Feb;21(2):156–158.
  • Hachiya N, Sochocka M, Brzecka A, et al. Nuclear Envelope and Nuclear Pore Complexes in Neurodegenerative Diseases—New Perspectives for Therapeutic Interventions. Mol Neurobiol. 2021;58(3):983–995.
  • Nofrini V, Di Giacomo D, Mecucci C. Nucleoporin genes in human diseases. Eur J Hum Genet. 2016;24(10):1388–1395.
  • Xu S, Powers MA. Nuclear pore proteins and cancer. Semin Cell Dev Biol. 2009;20(5):620–630.
  • Freibaum BD, Lu Y, Lopez-Gonzalez R, et al. GGGGCC repeat expansion in C9orf72 compromises nucleocytoplasmic transport. Nature. 2015 Sep;525(7567):129–133.
  • Zhang K, Donnelly CJ, Haeusler AR, et al. The C9orf72 repeat expansion disrupts nucleocytoplasmic transport. Nature. 2015 Sep;525(7567):56–61.
  • Grima JC, Daigle JG, Arbez N, et al. Mutant Huntingtin Disrupts the Nuclear Pore Complex. Neuron. 2017;94(1):93–107.e6.
  • Liu K-Y, Shyu Y, Barbaro BA,et al. 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. 2015 Mar;24(6):1602–1616.
  • Eftekharzadeh B, Daigle JG, Kapinos LE, et al. Tau Protein Disrupts Nucleocytoplasmic Transport in Alzheimer’s Disease. Neuron. 2018;99(5):925–940.e7.
  • Zhang X, Chen S, Yoo S, et al. Mutation in Nuclear Pore Component NUP155 Leads to Atrial Fibrillation and Early Sudden Cardiac Death. Cell. 2008;135(6):1017–1027.
  • Tarazó E, Rivera N,M, Roselló-Lletí E, et al. Heart Failure Induces Significant Changes in Nuclear Pore Complex of. Cardiomyocytes,” H PLoS One. 2012;7(11):48957.
  • Xu L, Pan L, Li J, et al. Nucleoporin 35 regulates cardiomyocyte pH homeostasis by controlling Na + -H + exchanger-1 expression. J Mol Cell Biol. 2015 Oct;7(5):476–485.
  • Legrand JMD, Hobbs RM. RNA processing in the male germline: mechanisms and implications for fertility. Semin Cell Dev Biol. 2018Jul;79:80–91.
  • Kroon E, Thorsteinsdottir U, Mayotte N, et al. NUP98-HOXA9 expression in hemopoietic stem cells induces chronic and acute myeloid leukemias in mice. EMBO J. 2001;20(3):350–361.
  • Borrow J, Shearman AM, Stanton VP, et al. The t(7;11)(p15;p15) translocation in acute myeloid leukaemia fuses the genes for nucleoporin NUP96 and class I homeoprotein HOXA9. Nat Genet. 1996 Feb;12(2):159–167.
  • Nakamura T, Largaespada DA, Lee MP, et al. Fusion of the nucleoporin gene NUP98 to HOXA9 by the chromosome translocation t(7;11)(p15;p15) in human myeloid leukaemia. Nat Genet. 1996 Feb;12(2):154–158.
  • Martínez N, Alons A, Moragues MD, et al. The Nuclear Pore Complex Protein Nup88 Is Overexpressed in Tumor Cells1. Cancer Res. 1999 Nov;59(21):5408–5411.
  • Li J, Zhao J, Li Y. Multiple biological processes may be associated with tumorigenesis under NUP88-overexpressed condition. Genes Chromosomes Cancer. 2017 Feb;56(2):117–127.
  • Naylor RM, Jeganathan KB, Cao X, et al. Nuclear pore protein NUP88 activates anaphase-promoting complex to promote aneuploidy. J Clin Investig. 2016;126(2):543–559.
  • Knowles RB, Sabry JH, Martone ME, et al. Translocation of RNA granules in living neurons. J Neurosci. 1996;16(24):7812–7820.
  • Fernandopulle MS, Lippincott-Schwartz J, Ward ME. RNA transport and local translation in neurodevelopmental and neurodegenerative disease. Nat Neurosci. 2021;24(5):622–632.
  • Alami NH, Smith RB, Carrasco MA, et al. Axonal Transport of TDP-43 mRNA Granules Is Impaired by ALS-Causing Mutations. Neuron. 2014;81(3):536–543.
  • Fallini C, Donlin-Asp PG, Rouanet JP, et al. Deficiency of the Survival of Motor Neuron Protein Impairs mRNA Localization and Local Translation in the Growth Cone of Motor Neurons. J Neurosci. 2016 Mar;36(13):3811–3820.
  • Iwahashi CK, Yasui DH, An H-J, et al. Protein composition of the intranuclear inclusions of FXTAS. Brain. 2006;129(1):256–271.
  • Shashidharan P, Sandu D, Potla U, et al. Transgenic mouse model of early-onset DYT1 dystonia. Hum Mol Genet. 2005;14(1):125–133.
  • Balch WE, Morimoto RI, Dillin A, et al. Adapting proteostasis for disease intervention. Sci (1979). 2008;319(5865):916–919.
  • Guo N, Peng Z. MG132, a proteasome inhibitor, induces apoptosis in tumor cells. Asia Pac J Clin Oncol. 2013 Mar;9(1):6–11.
  • Zavodszky E, Seaman MN, Moreau K, et al. Mutation in VPS35 associated with Parkinson’s disease impairs WASH complex association and inhibits autophagy. Nat Commun. 2014 May;5(1):3828.
  • McGough IJ, Steinberg F, Jia D, et al. Retromer binding to FAM21 and the WASH complex is perturbed by the Parkinson disease-linked VPS35(D620N) mutation. Curr Biol. 2014;24(14):1670–1676.
  • Nordgard SH, Johansen FE, Alnaes GIG, et al. Genome-wide analysis identifies 16q deletion associated with survival, molecular subtypes, mRNA expression, and germline haplotypes in breast cancer patients. Genes Chromosomes Cancer. 2008 Aug;47(8):680–696.
  • Boiteux S, Jinks-Robertson S. DNA repair mechanisms and the bypass of DNA damage in Saccharomyces cerevisiae. Genetics. 2013;193(4):1025–1064.
  • Wang Z, Zhang J. Abundant Indispensable Redundancies in Cellular Metabolic Networks. Genome Biol Evol. 2009;1:23–33.
  • Postigo A, Ramsden AE, Howell M, et al. Cytoplasmic ATR Activation Promotes Vaccinia Virus Genome Replication. Cell Rep. 2017 May;19(5):1022–1032.
  • Snetkov X, Weisswange I, Pfanzelter J, et al. NPF motifs in the vaccinia virus protein A36 recruit intersectin-1 to promote Cdc42: n-WASP-mediated viral release from infected cells. Nat Microbiol. 2016 Aug;1(10):16141.
  • Spruce AE, Breckenridge LJ, Lee AK, et al. Properties of the fusion pore that forms during exocytosis of a mast cell secretory vesicle. Neuron. 1990 May;4(5):643–654.
  • Breckenridge LJ, Almers W. Currents through the fusion pore that forms during exocytosis of a secretory vesicle. Nature. 1987 Aug;328(6133):814–817.
  • Zhang P. Rumschitzki D, Edwards RH. High-speed imaging reveals the bimodal nature of dense core vesicle exocytosis. Proceedings of the National Academy of Sciences. Jan. 2023;120(1):2017
  • Russell SJ, Steger KA, Johnston SA. Subcellular localization, stoichiometry, and protein levels of 26S proteasome subunits in yeast. J Biol Chem. 1999;274(31):21943–21952.
  • Reits EAJ, Benham AM, Plougastel B, et al. Dynamics of proteasome distribution in living cells. EMBO J. 1997;16(20):6087–6094.
  • Enenkel C, Kang RW, Wilfling F, et al. Intracellular localization of the proteasome in response to stress conditions. J Biol Chem. 2022;298(7):1–10.
  • Carvalho P, Goder V, Rapoport TA. Distinct Ubiquitin-Ligase Complexes Define Convergent Pathways for the Degradation of ER Proteins. Cell. 2006;126(2):361–373.
  • Smoyer CJ, Jaspersen SL. Patrolling the nucleus: inner nuclear membrane-associated degradation. Curr Genet. 2019;65(5):1099–1106.
  • Franić D, Zubčić K, Boban M. Nuclear ubiquitin-proteasome pathways in proteostasis maintenance. Biomolecules. 2021;11(1):1–16.