Mechanisms and functions of nuclear envelope remodelling

Nature Reviews Molecular Cell Biology

Volumn 18, Issue 4, 2017, Pages 229-245

  Ungricht, Rosemarie ^a   Kutay, Ulrike ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

LAMIN A; RIBONUCLEOPROTEIN;

AGING; CELL DIFFERENTIATION; CELL DIVISION; CELL GROWTH; CELL NUCLEUS MEMBRANE; CELL PLASTICITY; CYTOPLASM; GAMETOGENESIS; HUMAN; MITOSIS; MUSCULAR DYSTROPHY; NEUROMUSCULAR JUNCTION; NEUTROPHIL; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; REVIEW; VIRUS CAPSID; ANIMAL; CELL MOTION; METABOLISM; NUCLEOCYTOPLASMIC TRANSPORT; PHYSIOLOGY;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CAPSID; CELL DIFFERENTIATION; CELL MOVEMENT; HUMANS; MITOSIS; NEUTROPHILS; NUCLEAR ENVELOPE;

EID: 85010903664     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm.2016.153     Document Type: Review

References (210)

1. Knockenhauer K. E, & Schwartz T. U. The nuclear pore complex as a flexible and dynamic gate. Cell 164, 1162-1171 (2016).
2. Terry L. J, & Wente S. R. Flexible gates: dynamic topologies and functions for FG nucleoporins in nucleocytoplasmic transport. Eukaryot. Cell 8, 1814-1827 (2009).
3. Starr D. A, & Fridolfsson H. N. Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu. Rev. Cell Dev. Biol. 26, 421-444 (2010).
4. Sosa B. A, Kutay U, & Schwartz T. U. Structural insights into LINC complexes. Curr. Opin. Struct. Biol. 23, 285-291 (2013).
5. Gruenbaum Y, & Foisner R. Lamins: nuclear intermediate filament proteins with fundamental functions in nuclear mechanics and genome regulation. Annu. Rev. Biochem. 84, 131-164 (2015).
6. Koreny L, & Field M. C. Ancient eukaryotic origin and evolutionary plasticity of nuclear lamina. Genome Biol. Evol. 8, 2663-2671 (2016).
7. Burke B, & Stewart C. L. The nuclear lamins: flexibility in function. Nat. Rev. Mol. Cell Biol. 14, 13-24 (2013).
8. Shimi T, et al. The A-And B type nuclear lamin networks: microdomains involved in chromatin organization and transcription. Genes Dev. 22, 3409-3421 (2008).
9. Guelen L, et al. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453, 948-951 (2008).
10. Towbin B. D, Gonzalez-Sandoval A, & Gasser S. M. Mechanisms of heterochromatin subnuclear localization. Trends Biochem. Sci. 38, 356-363 (2013).
11. Kind J, & van Steensel B. Genome-nuclear lamina interactions and gene regulation. Curr. Opin. Cell Biol. 22, 320-325 (2010).
12. Hellberg T, Passvogel L, Schulz K. S, Klupp B. G, & Mettenleiter T. C. Nuclear egress of herpesviruses: the prototypic vesicular nucleocytoplasmic transport. Adv. Virus Res. 94, 81-140 (2016).
13. Speese S. D, et al. Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling. Cell 149, 832-846 (2012).
14. Maeshima K, et al. Nuclear pore formation but not nuclear growth is governed by cyclin-dependent kinases (Cdks) during interphase. Nat. Struct. Mol. Biol. 17, 1065-1071 (2010).
15. Dultz E, & Ellenberg J. Live imaging of single nuclear pores reveals unique assembly kinetics and mechanism in interphase. J. Cell Biol. 191, 15-22 (2010).
16. Zuleger N, et al. System analysis shows distinct mechanisms and common principles of nuclear envelope protein dynamics. J. Cell Biol. 193, 109-123 (2011).
17. Soullam B, & Worman H. J. Signals and structural features involved in integral membrane protein targeting to the inner nuclear membrane. J. Cell Biol. 130, 15-27 (1995).
18. Ungricht R, Klann M, Horvath P, & Kutay U. Diffusion and retention are major determinants of protein targeting to the inner nuclear membrane. J. Cell Biol. 209, 687-703 (2015).
19. Boni A, et al. Live imaging and modeling of inner nuclear membrane targeting reveals its molecular requirements in mammalian cells. J. Cell Biol. 209, 705-720 (2015).
20. Kralt A, et al. Conservation of inner nuclear membrane targeting sequences in mammalian Pom121 and yeast Heh2 membrane proteins. Mol. Biol. Cell 26, 3301-3312 (2015).
21. Meinema A. C, et al. Long unfolded linkers facilitate membrane protein import through the nuclear pore complex. Science 333, 90-93 (2011).
22. Funakoshi T, Clever M, Watanabe A, & Imamoto N. Localization of Pom121 to the inner nuclear membrane is required for an early step of interphase nuclear pore complex assembly. Mol. Biol. Cell 22, 1058-1069 (2011).
23. Yavuz S, et al. NLS-mediated NPC functions of the nucleoporin Pom121. FEBS Lett. 584, 3292-3298 (2010).
24. Doucet C. M, Talamas J. A, & Hetzer M. W. Cell cycle-dependent differences in nuclear pore complex assembly in metazoa. Cell 141, 1030-1041 (2010).
25. Makio T, et al. The nucleoporins Nup170p and Nup157p are essential for nuclear pore complex assembly. J. Cell Biol. 185, 459-473 (2009).
26. Scarcelli J. J, Hodge C. A, & Cole C. N. The yeast integral membrane protein Apq12 potentially links membrane dynamics to assembly of nuclear pore complexes. J. Cell Biol. 178, 799-812 (2007).
27. Wente S. R, & 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. 123, 275-284 (1993).
28. Onischenko E, Stanton L. H, Madrid A. S, Kieselbach T, & Weis K. Role of the Ndc1 interaction network in yeast nuclear pore complex assembly and maintenance. J. Cell Biol. 185, 475-491 (2009).
29. Otsuka S, et al. Nuclear pore assembly proceeds by an inside-out extrusion of the nuclear envelope. eLife 5, e19071 (2016).
30. Talamas J. A, & Hetzer M. W. POM121 and Sun1 play a role in early steps of interphase NPC assembly. J. Cell Biol. 194, 27-37 (2011).
31. Vollmer B, et al. Nup153 recruits the Nup107-160 complex to the inner nuclear membrane for interphasic nuclear pore complex assembly. Dev. Cell 33, 717-728 (2015).
32. Mitchell J. M, Mansfeld J, Capitanio J, Kutay U, & Wozniak R. W. Pom121 links two essential subcomplexes of the nuclear pore complex core to the membrane. J. Cell Biol. 191, 505-521 (2010).
33. Mészáros N, et al. Nuclear pore basket proteins are tethered to the nuclear envelope and can regulate membrane curvature. Dev. Cell 33, 285-298 (2015).
34. Vollmer B, et al. Dimerization and direct membrane interaction of Nup53 contribute to nuclear pore complex assembly. EMBO J. 31, 4072-4084 (2012).
35. Drin G, et al. A general amphipathic α-helical motif for sensing membrane curvature. Nat. Struct. Mol. Biol. 14, 138-146 (2007).
36. Dawson T. R, Lazarus M. D, Hetzer M. W, & Wente S. R. ER membrane-bending proteins are necessary for de novo nuclear pore formation. J. Cell Biol. 184, 659-675 (2009).
37. Zhang D, & Oliferenko S. Tts1, the fission yeast homologue of the TMEM33 family, functions in NE remodeling during mitosis. Mol. Biol. Cell 25, 2970-2983 (2014).
38. Chadrin A, et al. Pom33, a novel transmembrane nucleoporin required for proper nuclear pore complex distribution. J. Cell Biol. 189, 795-811 (2010).
39. Boban M, Pantazopoulou M, Schick A, Ljungdahl P. O, & Foisner R. A nuclear ubiquitin-proteasome pathway targets the inner nuclear membrane protein Asi2 for degradation. J. Cell Sci. 127, 3603-3613 (2014).
40. Deng M, & Hochstrasser M. Spatially regulated ubiquitin ligation by an ER/nuclear membrane ligase. Nature 443, 827-831 (2006).
41. Khmelinskii A, et al. Protein quality control at the inner nuclear membrane. Nature 516, 410-413 (2014).
42. Foresti O, Rodriguez-Vaello V, Funaya C, & Carvalho P. Quality control of inner nuclear membrane proteins by the Asi complex. Science 346, 751-755 (2014).
43. Zargari A, et al. Inner nuclear membrane proteins Asi1, Asi2, and Asi3 function in concert to maintain the latent properties of transcription factors Stp1 and Stp2. J. Biol. Chem. 282, 594-605 (2007).
44. Zattas D, Berk J. M, Kreft S. G, & Hochstrasser M. A. Conserved C terminal element in the yeast Doa10 and human MARCH6 ubiquitin ligases required for selective substrate degradation. J. Biol. Chem. 291, 12105-12118 (2016).
45. Coyaud E, et al. BioID-based identification of Skp Cullin F box (SCF)β-TrCP1/2 E3 ligase substrates. Mol. Cell. Proteomics 14, 1781-1795 (2015).
46. Toyama B. H, et al. Identification of long-lived proteins reveals exceptional stability of essential cellular structures. Cell 154, 971-982 (2013).
47. Savas J. N, Toyama B. H, Xu T, Yates J. R, & Hetzer M. W. Extremely long-lived nuclear pore proteins in the rat brain. Science 335, 942 (2012).
48. D Angelo M. A, Raices M, Panowski S. H, & Hetzer M. W. Age-dependent deterioration of nuclear pore complexes causes a loss of nuclear integrity in postmitotic cells. Cell 136, 284-295 (2009).
49. Mochida K, et al. Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus. Nature 522, 359-362 (2015).
50. Dou Z, et al. Autophagy mediates degradation of nuclear lamina. Nature 527, 105-109 (2015).
51. Lenain C, Gusyatiner O, Douma S, van den Broek B, & Peeper D. S. Autophagy-mediated degradation of nuclear envelope proteins during oncogene-induced senescence. Carcinogenesis 36, 1263-1274 (2015).
52. Ivanov A, et al. Lysosome-mediated processing of chromatin in senescence. J. Cell Biol. 202, 129-143 (2013).
53. Swift J, et al. Nuclear lamin A scales with tissue stiffness and enhances matrix-directed differentiation. Science 341, 1240104 (2013).
54. Harada T, et al. Nuclear lamin stiffness is a barrier to 3D migration, but softness can limit survival. J. Cell Biol. 204, 669-682 (2014).
55. Shin J. W, et al. Lamins regulate cell trafficking and lineage maturation of hematopoietic cells. Proc. Natl Acad. Sci. USA 110, 18892-18897 (2013).
56. Rowat A. C, et al. Nuclear envelope composition determines the ability of neutrophil-Type cells to passage through micron-scale constrictions. J. Biol. Chem. 288, 8610-8618 (2013).
57. Lombardi M. L, et al. The interaction between nesprins and sun proteins at the nuclear envelope is critical for force transmission between the nucleus and cytoskeleton. J. Biol. Chem. 286, 26743-26753 (2011).
58. Schreiner S. M, Koo P. K, Zhao Y, Mochrie S. G. J, & King M. C. The tethering of chromatin to the nuclear envelope supports nuclear mechanics. Nat. Commun. 6, 7159 (2015).
59. Furusawa T, et al. Chromatin decompaction by the nucleosomal binding protein HMGN5 impairs nuclear sturdiness. Nat. Commun. 6, 6138 (2015).
60. Guilluy C, et al. Isolated nuclei adapt to force and reveal a mechanotransduction pathway in the nucleus. Nat. Cell Biol. 16, 376-381 (2014).
61. Ihalainen T. O, et al. Differential basal to apical accessibility of lamin A/C epitopes in the nuclear lamina regulated by changes in cytoskeletal tension. Nat. Mater. 14, 1252-1261 (2015).
62. Versaevel M, et al. Super-resolution microscopy reveals LINC complex recruitment at nuclear indentation sites. Sci. Rep. 4, 7362 (2014).
63. Chambliss A. B, et al. The LINC-Anchored actin cap connects the extracellular milieu to the nucleus for ultrafast mechanotransduction. Sci. Rep. 3, 1087 (2013).
64. Fedorchak G. R, Kaminski A, & Lammerding J. Cellular mechanosensing: getting to the nucleus of it all. Prog. Biophys. Mol. Biol. 115, 76-92 (2014).
65. Ho C. Y, Jaalouk D. E, Vartiainen M. K, & Lammerding J. Lamin A/C and emerin regulate MKL1 SRF activity by modulating actin dynamics. Nature 497, 507-511 (2013).
66. Holaska J. M, Rais-Bahrami S, & Wilson K. L. Lmo7 is an emerin-binding protein that regulates the transcription of emerin and many other muscle-relevant genes. Hum. Mol. Genet. 15, 3459-3472 (2006).
67. Qi Y. X, et al. Nuclear envelope proteins modulate proliferation of vascular smooth muscle cells during cyclic stretch application. Proc. Natl Acad. Sci. USA 113, 5293-5298 (2016).
68. Han Y, et al. Nuclear envelope proteins Nesprin2 and LaminA regulate proliferation and apoptosis of vascular endothelial cells in response to shear stress. Biochim. Biophys. Acta 1853, 1165-1173 (2015).
69. Gundersen G. G, & Worman H. J. Nuclear positioning. Cell 152, 1376-1389 (2013).
70. Luxton G. W. G, Gomes E. R, Folker E. S, Vintinner E, & Gundersen G. G. Linear arrays of nuclear envelope proteins harness retrograde actin flow for nuclear movement. Science 329, 956-959 (2010).
71. Raab M, et al. ESCRT III repairs nuclear envelope ruptures during cell migration to limit DNA damage and cell death. Science 352, 359-362 (2016).
72. Denais C. M, et al. Nuclear envelope rupture and repair during cancer cell migration. Science 352, 353-358 (2016).
73. De Vos W. H, et al. Repetitive disruptions of the nuclear envelope invoke temporary loss of cellular compartmentalization in laminopathies. Hum. Mol. Genet. 20, 4175-4186 (2011).
74. Chial H. J, Rout M. P, Giddings T. H. Jr & Winey M. Saccharomyces cerevisiae Ndc1p is a shared component of nuclear pore complexes and spindle pole bodies. J. Cell Biol. 143, 1789-1800 (1998).
75. Casey A. K, et al. Integrity and function of the Saccharomyces cerevisiae spindle pole body depends on connections between the membrane proteins Ndc1, Rtn1, and Yop1. Genetics 192, 441-455 (2012).
76. Kupke T, et al. Targeting of Nbp1 to the inner nuclear membrane is essential for spindle pole body duplication. EMBO J. 30, 3337-3352 (2011).
77. Tamm T, et al. Brr6 drives the Schizosaccharomyces pombe spindle pole body nuclear envelope insertion/ extrusion cycle. J. Cell Biol. 195, 467-484 (2011).
78. Witkin K. L, Friederichs J. M, Cohen-Fix O, & Jaspersen S. L. Changes in the nuclear envelope environment affect spindle pole body duplication in Saccharomyces cerevisiae. Genetics 186, 867-883 (2010).
79. Makarova M, et al. Temporal regulation of lipin activity diverged to account for differences in mitotic programs. Curr. Biol. 26, 237-243 (2016).
80. Dultz E, et al. Systematic kinetic analysis of mitotic dis-And reassembly of the nuclear pore in living cells. J. Cell Biol. 180, 857-865 (2008).
81. Laurell E, et al. Phosphorylation of Nup98 by multiple kinases is crucial for NPC disassembly during mitotic entry. Cell 144, 539-550 (2011).
82. Molitor T. P, & Traktman P. Depletion of the protein kinase VRK1 disrupts nuclear envelope morphology and leads to BAF retention on mitotic chromosomes. Mol. Biol. Cell 25, 891-903 (2014).
83. Gorjánácz M, et al. Caenorhabditis elegans BAF 1 and its kinase VRK 1 participate directly in post-mitotic nuclear envelope assembly. EMBO J. 26, 132-143 (2007).
84. Hirota T, Lipp J. J, Toh B. H, & Peters J. M. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature 438, 1176-1180 (2005).
85. Tseng L. C, & Chen R. H. Temporal control of nuclear envelope assembly by phosphorylation of lamin B receptor. Mol. Biol. Cell 22, 3306-3317 (2011).
86. Gerace L, & Blobel G. The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell 19, 277-287 (1980).
87. Goss V. L, et al. Identification of nuclear βII protein kinase C as a mitotic lamin kinase. J. Biol. Chem. 269, 19074-19080 (1994).
88. Peter M, Nakagawa J, Dorée M, Labbé J. C, & Nigg E. A. In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase. Cell 61, 591-602 (1990).
89. Heald R, & McKeon F. Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 61, 579-589 (1990).
90. Mall M, et al. Mitotic lamin disassembly is triggered by lipid-mediated signaling. J. Cell Biol. 198, 981-990 (2012).
91. Gorjánácz M, & Mattaj I. W. Lipin is required for efficient breakdown of the nuclear envelope in Caenorhabditis elegans. J. Cell Sci. 122, 1963-1969 (2009).
92. Golden A, Liu J, & Cohen-Fix O. Inactivation of the C. elegans lipin homolog leads to ER disorganization and to defects in the breakdown and reassembly of the nuclear envelope. J. Cell Sci. 122, 1970-1978 (2009).
93. Bahmanyar S, et al. Spatial control of phospholipid flux restricts endoplasmic reticulum sheet formation to allow nuclear envelope breakdown. Genes Dev. 28, 121-126 (2014).
94. Raaijmakers J. A, et al. Nuclear envelope-Associated dynein drives prophase centrosome separation and enables Eg5 independent bipolar spindle formation. EMBO J. 31, 4179-4190 (2012).
95. De Simone A, Nédélec F, & Gönczy P. Dynein transmits polarized actomyosin cortical flows to promote centrosome separation. Cell Rep. 14, 2250-2262 (2016).
96. Splinter D, et al. Bicaudal D2, dynein, and kinesin 1 associate with nuclear pore complexes and regulate centrosome and nuclear positioning during mitotic entry. PLoS Biol. 8, e1000350 (2010).
97. Bolhy -Rfsti, et al. A Nup133 dependent NPC-Anchored network tethers centrosomes to the nuclear envelope in prophase. J. Cell Biol. 192, 855-871 (2011).
98. Beaudouin J, Gerlich D, Daigle N, Eils R, & Ellenberg J. Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina. Cell 108, 83-96 (2002).
99. Salina D, et al. Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell 108, 97-107 (2002).
100. Turgay Y, et al. SUN proteins facilitate the removal of membranes from chromatin during nuclear envelope breakdown. J. Cell Biol. 204, 1099-1109 (2014).
101. Mühlhäusser P, & Kutay U. An in vitro nuclear disassembly system reveals a role for the RanGTPase system and microtubule-dependent steps in nuclear envelope breakdown. J. Cell Biol. 178, 595-610 (2007).
102. Schlaitz A. L, Thompson J, Wong C. C. L, Yates J. R, & Heald R. REEP3/4 ensure endoplasmic reticulum clearance from metaphase chromatin and proper nuclear envelope architecture. Dev. Cell 26, 315-323 (2013).
103. Schweizer N, Pawar N, Weiss M, & Maiato H. An organelle-exclusion envelope assists mitosis and underlies distinct molecular crowding in the spindle region. J. Cell Biol. 210, 695-704 (2015).
104. Ulbert S, Platani M, Boue S, & Mattaj I. W. Direct membrane protein-DNA interactions required early in nuclear envelope assembly. J. Cell Biol. 173, 469-476 (2006).
105. Anderson D. J, Vargas J. D, Hsiao J. P, & Hetzer M. W. Recruitment of functionally distinct membrane proteins to chromatin mediates nuclear envelope formation in vivo. J. Cell Biol. 186, 183-191 (2009).
106. Haraguchi T, et al. Live cell imaging and electron microscopy reveal dynamic processes of BAF-directed nuclear envelope assembly. J. Cell Sci. 121, 2540-2554 (2008).
107. Schooley A, Moreno-Andrés D, De Magistris P, Vollmer B, & Antonin W. The lysine demethylase LSD1 is required for nuclear envelope formation at the end of mitosis. J. Cell Sci. 128, 3466-3477 (2015).
108. Afonso O, et al. Feedback control of chromosome separation by a midzone Aurora B gradient. Science 345, 332-336 (2014).
109. Vagnarelli P, et al. Repo-Man coordinates chromosomal reorganization with nuclear envelope reassembly during mitotic exit. Dev. Cell 21, 328-342 (2011).
110. Ramadan K, et al. Cdc48/p97 promotes reformation of the nucleus by extracting the kinase Aurora B from chromatin. Nature 450, 1258-1262 (2007).
111. Fischle W, et al. Regulation of HP1 chromatin binding by histone H3 methylation and phosphorylation. Nature 438, 1116-1122 (2005).
112. Wandke C, & Kutay U. Enclosing chromatin: reassembly of the nucleus after open mitosis. Cell 152, 1222-1225 (2013).
113. Antonin W, Franz C, Haselmann U, Antony C, & Mattaj I. W. The integral membrane nucleoporin pom121 functionally links nuclear pore complex assembly and nuclear envelope formation. Mol. Cell 17, 83-92 (2005).
114. Walther T. C, et al. The conserved Nup107-160 complex is critical for nuclear pore complex assembly. Cell 113, 195-206 (2003).
115. Harel A, et al. Removal of a single pore subcomplex results in vertebrate nuclei devoid of nuclear pores. Mol. Cell 11, 853-864 (2003).
116. Zierhut C, Jenness C, Kimura H, & Funabiki H. Nucleosomal regulation of chromatin composition and nuclear assembly revealed by histone depletion. Nat. Struct. Mol. Biol. 21, 617-625 (2014).
117. Inoue A, & Zhang Y. Nucleosome assembly is required for nuclear pore complex assembly in mouse zygotes. Nat. Struct. Mol. Biol. 21, 609-616 (2014).
118. Franz C, et al. MEL 28/ELYS is required for the recruitment of nucleoporins to chromatin and postmitotic nuclear pore complex assembly. EMBO Rep. 8, 165-172 (2007).
119. Rasala B. A, Ramos C, Harel A, & Forbes D. J. Capture of AT rich chromatin by ELYS recruits POM121 and NDC1 to initiate nuclear pore assembly. Mol. Biol. Cell 19, 3982-3996 (2008).
120. Hampoelz B, et al. Pre-Assembled nuclear pores insert into the nuclear envelope during early development. Cell 166, 664-678 (2016).
121. Anderson D. J, & Hetzer M. W. Nuclear envelope formation by chromatin-mediated reorganization of the endoplasmic reticulum. Nat. Cell Biol. 9, 1160-1166 (2007).
122. Dechat T, et al. LAP2α and BAF transiently localize to telomeres and specific regions on chromatin during nuclear assembly. J. Cell Sci. 117, 6117-6128 (2004).
123. Mora-Bermúdez F, Gerlich D, & Ellenberg J. Maximal chromosome compaction occurs by axial shortening in anaphase and depends on Aurora kinase. Nat. Cell Biol. 9, 822-831 (2007).
124. Zhuang X, Semenova E, Maric D, & Craigie R. Dephosphorylation of barrier-To autointegration factor by protein phosphatase 4 and its role in cell mitosis. J. Biol. Chem. 289, 1119-1127 (2014).
125. Vietri M, et al. Spastin and ESCRT-III coordinate mitotic spindle disassembly and nuclear envelope sealing. Nature 522, 231-235 (2015).
126. Olmos Y, Hodgson L, Mantell J, Verkade P, & Carlton J. G. ESCRT-III controls nuclear envelope reformation. Nature 522, 236-239 (2015).
127. Olmos Y, Perdrix-Rosell A, & Carlton J. G. Membrane binding by CHMP7 coordinates ESCRT-III-dependent nuclear envelope reformation. Curr. Biol. 26, 2635-2641 (2016).
128. Hetzer M, et al. Distinct AAA-ATPase p97 complexes function in discrete steps of nuclear assembly. Nat. Cell Biol. 3, 1086-1091 (2001).
129. Dobrynin G, et al. Cdc48/p97-Ufd1-Npl4 antagonizes Aurora B during chromosome segregation in HeLa cells. J. Cell Sci. 124, 1571-1580 (2011).
130. Pante N, & Kann M. Nuclear pore complex is able to transport macromolecules with diameters of about 39 nm. Mol. Biol. Cell 13, 425-434 (2002).
131. Granzow H, et al. Egress of alphaherpesviruses: comparative ultrastructural study. J. Virol. 75, 3675-3684 (2001).
132. Park R, & Baines J. D. 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. 80, 494-504 (2006).
133. Muranyi W, Haas J, Wagner M, Krohne G, & Koszinowski U. H. Cytomegalovirus recruitment of cellular kinases to dissolve the nuclear lamina. Science 297, 854-857 (2002).
134. Reynolds A. E, et al. UL31 and UL34 proteins of herpes simplex virus type 1 form a complex that accumulates at the nuclear rim and is required for envelopment of nucleocapsids. J. Virol. 75, 8803-8817 (2001).
135. Klupp B. G, et al. Vesicle formation from the nuclear membrane is induced by coexpression of two conserved herpesvirus proteins. Proc. Natl Acad. Sci. USA 104, 7241-7246 (2007).
136. Bigalke J. M, & Heldwein E. E. Structural basis of membrane budding by the nuclear egress complex of herpesviruses. EMBO J. 34, 2921-2936 (2015).
137. Hagen C, et al. Structural basis of vesicle formation at the inner nuclear membrane. Cell 163, 1692-1701 (2015).
138. Zeev-Ben-Mordehai T, et al. Crystal structure of the herpesvirus nuclear egress complex provides insights into inner nuclear membrane remodeling. Cell Rep. 13, 2645-2652 (2015).
139. Lorenz M, et al. A single herpesvirus protein can mediate vesicle formation in the nuclear envelope. J. Biol. Chem. 290, 6962-6974 (2015).
140. Lee C. P, et al. The ESCRT machinery is recruited by the viral BFRF1 protein to the nucleus-Associated membrane for the maturation of Epstein-Barr Virus. PLoS Pathog. 8, e1002904 (2012).
141. Lee C. P, et al. The ubiquitin ligase Itch and ubiquitination regulate BFRF1 mediated nuclear envelope modification for Epstein-Barr virus maturation. J. Virol. 90, 8994-9007 (2016).
142. Maric M, et al. A functional role for TorsinA in herpes simplex virus 1 nuclear egress. J. Virol. 85, 9667-9679 (2011).
143. Turner E. M, Brown R. S. H, Laudermilch E, Tsai P. L, & Schlieker C. The Torsin activator LULL1 is required for efficient growth of HSV 1. J. Virol. 89, 8444-8452 (2015).
144. Sosa B. A, et al. How lamina-Associated polypeptide 1 (LAP1) activates Torsin. eLife 3, e03239 (2014).
145. Brown R. S. H, Zhao C, Chase A. R, Wang J, & Schlieker C. The mechanism of Torsin ATPase activation. Proc. Natl Acad. Sci. USA 111, E4822-E4831 (2014).
146. Jokhi V, et al. Torsin mediates primary envelopment of large ribonucleoprotein granules at the nuclear envelope. Cell Rep. 3, 988-995 (2013).
147. Naismith T. V, Heuser J. E, Breakefield X. O, & Hanson P. I. TorsinA in the nuclear envelope. Proc. Natl Acad. Sci. USA 101, 7612-7617 (2004).
148. Goodchild R. E, Kim C. E, & Dauer W. T. Loss of the dystonia-Associated protein torsinA selectively disrupts the neuronal nuclear envelope. Neuron 48, 923-932 (2005).
149. Kim C. E, Perez A, Perkins G, Ellisman M. H, & Dauer W. T. A molecular mechanism underlying the neural-specific defect in torsinA mutant mice. Proc. Natl Acad. Sci. USA 107, 9861-9866 (2010).
150. Liang C. C, Tanabe L. M, Jou S, Chi F, & Dauer W. T. TorsinA hypofunction causes abnormal twisting movements and sensorimotor circuit neurodegeneration. J. Clin. Invest. 124, 3080-3092 (2014).
151. Mattout A, Cabianca D. S, & Gasser S. M. Chromatin states and nuclear organization in development -A view from the nuclear lamina. Genome Biol. 16, 284-215 (2015).
152. Solovei I, et al. LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 152, 584-598 (2013).
153. Peric-Hupkes D, et al. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol. Cell 38, 603-613 (2010).
154. Zullo J. M, et al. DNA sequence-dependent compartmentalization and silencing of chromatin at the nuclear lamina. Cell 149, 1474-1487 (2012).
155. Szczerbal I, Foster H. A, & Bridger J. M. The spatial repositioning of adipogenesis genes is correlated with their expression status in a porcine mesenchymal stem cell adipogenesis model system. Chromosoma 118, 647-663 (2009).
156. Robson M. I, et al. Tissue-specific gene repositioning by muscle nuclear membrane proteins enhances repression of critical developmental genes during myogenesis. Mol. Cell 62, 834-847 (2016).
157. Zuleger N, et al. Specific nuclear envelope transmembrane proteins can promote the location of chromosomes to and from the nuclear periphery. Genome Biol. 14, R14 (2013).
158. Wong X, Luperchio T. R, & Reddy K. L. NET gains and losses: the role of changing nuclear envelope proteomes in genome regulation. Curr. Opin. Cell Biol. 28, 105-120 (2014).
159. Worman H. J, & Schirmer E. C. Nuclear membrane diversity: underlying tissue-specific pathologies in disease?. Curr. Opin. Cell Biol. 34, 101-112 (2015).
160. Huber M. D, Guan T, & Gerace L. Overlapping functions of nuclear envelope proteins NET25 (Lem2) and emerin in regulation of extracellular signal-regulated kinase signaling in myoblast differentiation. Mol. Cell. Biol. 29, 5718-5728 (2009).
161. Chen I. H. B, Huber M, Guan T, Bubeck A, & Gerace L. Nuclear envelope transmembrane proteins (NETs) that are up regulated during myogenesis. BMC Cell Biol. 7, 1 (2006).
162. Burke B, & Stewart C. L. Functional architecture of the cell s nucleus in development, aging, and disease. Curr. Top. Dev. Biol. 109, 1-52 (2014).
163. Favreau C, Higuet D, Courvalin J. C, & Buendia B. Expression of a mutant lamin A that causes Emery-Dreifuss muscular dystrophy inhibits in vitro differentiation of C2C12 myoblasts. Mol. Cell. Biol. 24, 1481-1492 (2004).
164. Perovanovic J, et al. Laminopathies disrupt epigenomic developmental programs and cell fate. Sci. Transl Med. 8, 335ra58 (2016).
165. Bakay M, et al. Nuclear envelope dystrophies show a transcriptional fingerprint suggesting disruption of Rb-MyoD pathways in muscle regeneration. Brain 129, 996-1013 (2006).
166. Melcon G, et al. Loss of emerin at the nuclear envelope disrupts the Rb1/E2F and MyoD pathways during muscle regeneration. Hum. Mol. Genet. 15, 637-651 (2006).
167. Frock R. L, et al. Lamin A/C and emerin are critical for skeletal muscle satellite cell differentiation. Genes Dev. 20, 486-500 (2006).
168. Méjat A, et al. Lamin A/C mediated neuromuscular junction defects in Emery-Dreifuss muscular dystrophy. J. Cell Biol. 184, 31-44 (2009).
169. Grady R. M, Starr D. A, Ackerman G. L, Sanes J. R, & Han M. Syne proteins anchor muscle nuclei at the neuromuscular junction. Proc. Natl Acad. Sci. USA 102, 4359-4364 (2005).
170. Zhang X, et al. Syne 1 and Syne 2 play crucial roles in myonuclear anchorage and motor neuron innervation. Development 134, 901-908 (2007).
171. Lei K, et al. SUN1 and SUN2 play critical but partially redundant roles in anchoring nuclei in skeletal muscle cells in mice. Proc. Natl Acad. Sci. USA 106, 10207-10212 (2009).
172. Gros-Louis F, et al. Mutations in SYNE1 lead to a newly discovered form of autosomal recessive cerebellar ataxia. Nat. Genet. 39, 80-85 (2007).
173. Hoffmann K, et al. Mutations in the gene encoding the lamin B receptor produce an altered nuclear morphology in granulocytes (Pelger-Huët anomaly). Nat. Genet. 31, 410-414 (2002).
174. Gravemann S, et al. Dosage effect of zero to three functional LBR-genes in vivo and in vitro. Nucleus 1, 179-189 (2010).
175. Penkner A, et al. The nuclear envelope protein Matefin/SUN 1 is required for homologous pairing in C. elegans meiosis. Dev. Cell 12, 873-885 (2007).
176. Horn H. -Rffrt, et al. A mammalian KASH domain protein coupling meiotic chromosomes to the cytoskeleton. J. Cell Biol. 202, 1023-1039 (2013).
177. Morimoto -Rfaut, et al. A conserved KASH domain protein associates with telomeres, SUN1, and dynactin during mammalian meiosis. J. Cell Biol. 198, 165-172 (2012).
178. Ding X, et al. SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev. Cell 12, 863-872 (2007).
179. Lee C. Y, et al. Mechanism and regulation of rapid telomere prophase movements in mouse meiotic chromosomes. Cell Rep. 11, 551-563 (2015).
180. Jahn D, Schramm S, Benavente R, & Alsheimer M. Dynamic properties of meiosis-specific lamin C2 and its impact on nuclear envelope integrity. Nucleus 1, 273-283 (2010).
181. Link J, et al. The meiotic nuclear lamina regulates chromosome dynamics and promotes efficient homologous recombination in the mouse. PLoS Genet. 9, e1003261 (2013).
182. Göb E, Schmitt J, Benavente R, & Alsheimer M. Mammalian sperm head formation involves different polarization of two novel LINC complexes. PLoS ONE 5, e12072 (2010).
183. Frohnert C, Schweizer S, & Hoyer-Fender S. SPAG4L/SPAG4L 2 are testis-specific SUN domain proteins restricted to the apical nuclear envelope of round spermatids facing the acrosome. Mol. Hum. Reprod. 17, 207-218 (2011).
184. Calvi A, et al. SUN4 is essential for nuclear remodeling during mammalian spermiogenesis. Dev. Biol. 407, 321-330 (2015).
185. Pasch E, Link J, Beck C, Scheuerle S, & Alsheimer M. The LINC complex component Sun4 plays a crucial role in sperm head formation and fertility. Biol. Open 4, 1792-1802 (2015).
186. Webster B. M, Colombi P, Jäger J, & Lusk C. P. Surveillance of nuclear pore complex assembly by ESCRT-III/Vps4. Cell 159, 388-401 (2014).
187. Alonso Y, Adell M, Migliano S. M, & Teis D. ESCRT III and Vps4: a dynamic multipurpose tool for membrane budding and scission. FEBS J. 283, 3288-3302 (2016).
188. Kaganovich D, Kopito R, & Frydman J. Misfolded proteins partition between two distinct quality control compartments. Nature 454, 1088-1095 (2008).
189. Spokoini R, et al. Confinement to organelle-Associated inclusion structures mediates asymmetric inheritance of aggregated protein in budding yeast. Cell Rep. 2, 738-747 (2012).
190. Hill S. M, et al. Asymmetric inheritance of aggregated proteins and age reset in yeast are regulated by Vac17 dependent vacuolar functions. Cell Rep. 16, 826-838 (2016).
191. Saarikangas J, Barral Y, & Schekman R. Protein aggregates are associated with replicative aging without compromising protein quality control. eLife 4, e06197 (2015).
192. Zwerger M, et al. Myopathic lamin mutations impair nuclear stability in cells and tissue and disrupt nucleo cytoskeletal coupling. Hum. Mol. Genet. 22, 2335-2349 (2013).
193. Mewborn S. K, et al. Altered chromosomal positioning, compaction, and gene expression with a lamin A/C gene mutation. PLoS ONE 5, e14342 (2010).
194. Vadrot N, et al. The p.R482W substitution in A type lamins deregulates SREBP1 activity in Dunnigan-Type familial partial lipodystrophy. Hum. Mol. Genet. 24, 2096-2109 (2015).
195. Oldenburg A. R, Delbarre E, Thiede B, Vigouroux C, & Collas P. Deregulation of Fragile X related protein 1 by the lipodystrophic lamin A p. R482W mutation elicits a myogenic gene expression program in preadipocytes. Hum. Mol. Genet. 23, 1151-1162 (2014).
196. Navarro C. L, et al. Loss of ZMPSTE24 (FACE 1) causes autosomal recessive restrictive dermopathy and accumulation of lamin A precursors. Hum. Mol. Genet. 14, 1503-1513 (2005).
197. Agarwal A. K, Fryns J. P, Auchus R. J, & Garg A. Zinc metalloproteinase, ZMPSTE24, is mutated in mandibuloacral dysplasia. Hum. Mol. Genet. 12, 1995-2001 (2003).
198. De Sandre-Giovannoli A, et al. Lamin a truncation in Hutchinson-Gilford progeria. Science 300, 2055-2055 (2003).
199. Eriksson M, et al. Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423, 293-298 (2003).
200. Gordon L. B, Rothman F. G, López-Otín C, & Misteli T. Progeria: a paradigm for translational medicine. Cell 156, 400-407 (2014).
201. Kubben N, et al. Repression of the antioxidant NRF2 pathway in premature aging. Cell 165, 1361-1374 (2016).
202. Mostoslavsky R, et al. Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell 124, 315-329 (2006).
203. Ghosh S, Liu B, Wang Y, Hao Q, & Zhou Z. Lamin A is an endogenous SIRT6 activator and promotes SIRT6 mediated DNA repair. Cell Rep. 13, 1396-1406 (2015).
204. Puente X. S, et al. Exome sequencing and functional analysis identifies BANF1 mutation as the cause of a hereditary progeroid syndrome. Am. J. Hum. Genet. 88, 650-656 (2011).
205. Holaska J. M, Lee K. K, Kowalski A. K, & Wilson K. L. Transcriptional repressor germ cell-less (GCL) and barrier to autointegration factor (BAF) compete for binding to emerin in vitro. J. Biol. Chem. 278, 6969-6975 (2003).
206. Hatch E. M, Fischer A. H, Deerinck T. J, & Hetzer M. W. Catastrophic nuclear envelope collapse in cancer cell micronuclei. Cell 154, 47-60 (2013).
207. Crasta K, et al. DNA breaks and chromosome pulverization from errors in mitosis. Nature 482, 53-58 (2012).
208. Zhang C. Z, et al. Chromothripsis from DNA damage in micronuclei. Nature 522, 179-184 (2015).
209. Stephens P. J, et al. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144, 27-40 (2011).
210. von Appen A, et al. In situ structural analysis of the human nuclear pore complex. Nature 526, 140-143 (2015).