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Navigating the Nuclear Envelope: One or Multiple Transport Mechanisms for Integral Membrane Proteins?

  • Charles R. Dixon
  • Eric C. Schirmer
Chapter
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 33)

Abstract

Several different mechanisms have been proposed for how membrane proteins access the inner nuclear membrane. These include mechanisms using both the central and peripheral channels of the nuclear pore complexes that involve free diffusion in the membrane, directional transport using transport receptors, directional transport with inner nuclear membrane proteins acting as their own transport receptors, an ATP-dependent process, and mechanisms involving membrane fusion. However, whether the differences reported reflect fully distinct mechanisms, different licensing steps for the same fundamental mechanism, or artifacts of experimental manipulation remains unclear. It is also reasonable to postulate that the hardware for multiple mechanisms exists but that some are backup mechanisms only used if the primary mechanism fails. If such is the case, there is also to consider the biological context, nuclear pore architecture, abundance of relevant proteins and motifs, and energy expenditure for different or competing mechanisms. Here, we evaluate existing data supporting these proposed mechanisms in context of these factors, the milieu of inner nuclear membrane proteins and evolution.

References

  1. Acehan D, Santarella-Mellwig R, Devos DP (2014) A bacterial tubulovesicular network. J Cell Sci 127:277–280.  https://doi.org/10.1242/jcs.137596CrossRefPubMedGoogle Scholar
  2. Aitchison JD, Rout MP (2012) The yeast nuclear pore complex and transport through it. Genetics 190:855–883.  https://doi.org/10.1534/genetics.111.127803CrossRefPubMedPubMedCentralGoogle Scholar
  3. Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT, Rout MP, Sali A (2007a) Determining the architectures of macromolecular assemblies. Nature 450:683–694.  https://doi.org/10.1038/nature06404CrossRefPubMedGoogle Scholar
  4. Alber F, Dokudovskaya S, Veenhoff LM, Zhang W, Kipper J, Devos D, Suprapto A, Karni-Schmidt O, Williams R, Chait BT, Sali A, Rout MP (2007b) The molecular architecture of the nuclear pore complex. Nature 450:695–701.  https://doi.org/10.1038/nature06405CrossRefPubMedGoogle Scholar
  5. Allen NPC, Huang L, Burlingame A, Rexach M (2001) Proteomic analysis of nucleoporin interacting proteins. J Biol Chem 276:29268–29274.  https://doi.org/10.1074/jbc.M102629200CrossRefPubMedGoogle Scholar
  6. Antonin W, Mattaj IW (2005) Nuclear pore complexes: round the bend? Nat Cell Biol 7:10–12.  https://doi.org/10.1038/ncb0105-10CrossRefPubMedGoogle Scholar
  7. Audhya A, Desai A, Oegema K (2007) A role for Rab5 in structuring the endoplasmic reticulum. J Cell Biol 178:43–56.  https://doi.org/10.1083/jcb.200701139CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bastos R, Lin A, Enarson M, Burke B (1996) Targeting and function in mRNA export of nuclear pore complex protein Nup153. J Cell Biol 134:1141–1156.  https://doi.org/10.1083/jcb.134.5.1141CrossRefPubMedGoogle Scholar
  9. Batrakou DG, Kerr ARW, Schirmer EC (2009) Comparative proteomic analyses of the nuclear envelope and pore complex suggests a wide range of heretofore unexpected functions. J Proteomics 72:56–70.  https://doi.org/10.1016/j.jprot.2008.09.004CrossRefPubMedGoogle Scholar
  10. Bayliss R, Littlewood T, Stewart M (2000) Structural basis for the interaction between FxFG nucleoporin repeats and importin-β in nuclear trafficking. Cell 102:99–108.  https://doi.org/10.1016/S0092-8674(00)00014-3CrossRefPubMedGoogle Scholar
  11. Ben-Efraim I, Gerace L (2001) Gradient of increasing affinity of importin beta for nucleoporins along the pathway of nuclear import. J Cell Biol 152:411–417CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bjerke SL, Roller RJ (2006) Roles for herpes simplex virus type 1 UL34 and US3 proteins in disrupting the nuclear lamina during herpes simplex virus type 1 egress. Virology 347:261–276.  https://doi.org/10.1016/j.virol.2005.11.053CrossRefPubMedPubMedCentralGoogle Scholar
  13. Boni A, Politi AZ, Strnad P, Xiang W, Hossain MJ, Ellenberg J (2015) Live imaging and modeling of inner nuclear membrane targeting reveals its molecular requirements in mammalian cells. J Cell Biol 209:705–720.  https://doi.org/10.1083/jcb.201409133CrossRefPubMedPubMedCentralGoogle Scholar
  14. Brachner A, Foisner R (2011) Evolvement of LEM proteins as chromatin tethers at the nuclear periphery. Biochem Soc Trans 39:1735–1741.  https://doi.org/10.1042/BST20110724CrossRefPubMedPubMedCentralGoogle Scholar
  15. Brachner A, Reipert S, Foisner R, Gotzmann J (2005) LEM2 is a novel MAN1-related inner nuclear membrane protein associated with A-type lamins. J Cell Sci 118:5797–5810.  https://doi.org/10.1242/jcs.02701CrossRefPubMedGoogle Scholar
  16. Braunagel SC, Williamson ST, Ding Q, Wu X, Summers MD (2007) Early sorting of inner nuclear membrane proteins is conserved. Proc Natl Acad Sci USA 104:9307–9312.  https://doi.org/10.1073/pnas.0703186104CrossRefPubMedGoogle Scholar
  17. Braunagel SC, Williamson ST, Saksena S, Zhong Z, Russell WK, Russell DH, Summers MD (2004) Trafficking of ODV-E66 is mediated via a sorting motif and other viral proteins: facilitated trafficking to the inner nuclear membrane. Proc Natl Acad Sci USA 101:8372–8377.  https://doi.org/10.1073/pnas.0402727101CrossRefPubMedGoogle Scholar
  18. Broers JLV, Peeters EAG, Kuijpers HJH, Endert J, Bouten CVC, Oomens CWJ, Baaijens FPT, Ramaekers FCS (2004) Decreased mechanical stiffness in LMNA-/- cells is caused by defective nucleo-cytoskeletal integrity: implications for the development of laminopathies. Hum Mol Genet 13:2567–2580.  https://doi.org/10.1093/hmg/ddh295CrossRefPubMedGoogle Scholar
  19. Buch C, Lindberg R, Figueroa R, Gudise S, Onischenko E, Hallberg E (2009) An integral protein of the inner nuclear membrane localizes to the mitotic spindle in mammalian cells. J Cell Sci 122:2100–2107.  https://doi.org/10.1242/jcs.047373CrossRefPubMedGoogle Scholar
  20. Bui KH, Von Appen A, Diguilio AL, Ori A, Sparks L, Mackmull MT, Bock T, Hagen W, Andrés-Pons A, Glavy JS, Beck M (2013) Integrated structural analysis of the human nuclear pore complex scaffold. Cell 155:1233–1243.  https://doi.org/10.1016/j.cell.2013.10.055CrossRefPubMedGoogle Scholar
  21. Burke B, Stewart CL (2013) The nuclear lamins: flexibility in function. Nat Rev Mol Cell Biol 14:13–24.  https://doi.org/10.1038/nrm3488CrossRefPubMedGoogle Scholar
  22. Callan HG, Randall JT, Tomlin SG (1949) An electron microscope study of the nuclear membrane. Nature 163:280–280.  https://doi.org/10.1038/163280a0CrossRefPubMedGoogle Scholar
  23. Carrion-Vazquez M, Oberhauser AF, Fowler SB, Marszalek PE, Broedel SE, Clarke J, Fernandez JM (1999) Mechanical and chemical unfolding of a single protein: a comparison. Proc Natl Acad Sci USA 96:3694–3699.  https://doi.org/10.1073/PNAS.96.7.3694CrossRefPubMedGoogle Scholar
  24. Chou PY, Fasman GD (1978) Empirical predictions of protein conformation. Ann Rev Biochem 47:251–276CrossRefPubMedGoogle Scholar
  25. Cingolani G, Petosa C, Weis K, Müller CW (1999) Structure of importin-beta bound to the IBB domain of importin-alpha. Nature 399:221–229.  https://doi.org/10.1038/20367CrossRefPubMedGoogle Scholar
  26. Clements L, Manilal S, Love DR, Morris GE (2000) Direct interaction between emerin and lamin A. Biochem Biophys Res Commun 267:709–714.  https://doi.org/10.1006/bbrc.1999.2023CrossRefPubMedGoogle Scholar
  27. Cronshaw JM (2002) Proteomic analysis of the mammalian nuclear pore complex. J Cell Biol 158:915–927.  https://doi.org/10.1083/jcb.200206106CrossRefPubMedPubMedCentralGoogle Scholar
  28. D’ Angelo MA, Anderson DJ, Richard E, Hetzer MW (2006) Nuclear pores form de novo from both sides of the nuclear envelope. Science 312:440–443.  https://doi.org/10.1126/science.1124196CrossRefGoogle Scholar
  29. Dacks JB, Field MC, Buick R, Eme L, Gribaldo S, Roger AJ, Brochier-Armanet C, Devos DP (2016) The changing view of eukaryogenesis – fossils, cells, lineages and how they all come together. J Cell Sci 129:3695–3703.  https://doi.org/10.1242/jcs.178566CrossRefPubMedGoogle Scholar
  30. de Las Heras JI, Meinke P, Batrakou DG, Srsen V, Zuleger N, Kerr AR, Schirmer EC (2013) Tissue specificity in the nuclear envelope supports its functional complexity. Nucleus 4:460–477.  https://doi.org/10.4161/nucl.26872CrossRefPubMedGoogle Scholar
  31. De vos WH, Houben F, Kamps M, Malhas A, Verheyen F, Cox J, Manders EMM, Verstraeten VLRM, Van steensel MAM, Marcelis CLM, Van den wijngaard A, Vaux DJ, Ramaekers FCS, Broers JLV (2011) Repetitive disruptions of the nuclear envelope invoke temporary loss of cellular compartmentalization in laminopathies. Hum Mol Genet 20:4175–4186.  https://doi.org/10.1093/hmg/ddr344CrossRefPubMedGoogle Scholar
  32. Demmerle J, Koch AJ, Holaska JM (2012) The nuclear envelope protein emerin binds directly to histone deacetylase 3 (HDAC3) and activates HDAC3 activity. J Biol Chem 287:22080–22088.  https://doi.org/10.1074/jbc.M111.325308CrossRefPubMedPubMedCentralGoogle Scholar
  33. Devos D, Dokudovskaya S, Alber F, Williams R, Chait BT, Sali A, Rout MP (2004) Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol 2(12):e80.  https://doi.org/10.1371/journal.pbio.0020380CrossRefGoogle Scholar
  34. Ellenberg J, Siggia ED, Moreira JE, Smith CL, Presley JF, Worman HJ, Lippincott-Schwartz J (1997) Nuclear membrane dynamics and reassembly in Living Cells: targeting of an inner nuclear membrane protein in interphase and mitosis. J Cell Biol 138(6):1193–1206CrossRefPubMedPubMedCentralGoogle Scholar
  35. Ellis DJ, Jenkins H, Whitfield WG, Hutchison CJ (1997) GST-lamin fusion proteins act as dominant negative mutants in Xenopus egg extract and reveal the function of the lamina in DNA replication. J Cell Sci 110:2507–2518PubMedGoogle Scholar
  36. Fahrenkrog B, Aebi U (2003) The nuclear pore complex: nucleocytoplasmic transport and beyond. Nat Rev Mol Cell Biol 4:757–766.  https://doi.org/10.1038/nrm1230CrossRefPubMedGoogle Scholar
  37. Faria PA, Chakraborty P, Levay A, Barber GN, Ezelle HJ, Enninga J, Arana C, van Deursen J, Fontoura BMA (2005) VSV disrupts the Rae1/mrnp41 mRNA nuclear export pathway. Mol Cell 17:93–102.  https://doi.org/10.1016/j.molcel.2004.11.023CrossRefPubMedGoogle Scholar
  38. Fiserova J, Richards SA, Wente SR, Goldberg MW (2010) Facilitated transport and diffusion take distinct spatial routes through the nuclear pore complex. J Cell Sci 123:2773–2780.  https://doi.org/10.1242/jcs.070730CrossRefPubMedPubMedCentralGoogle Scholar
  39. Foisner R, Gerace L (1993) Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation. Cell 73:1267–1279.  https://doi.org/10.1016/0092-8674(93)90355-TCrossRefPubMedGoogle Scholar
  40. Funakoshi T, Clever M, Watanabe A, Imamoto N (2011) 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.  https://doi.org/10.1091/mbc.E10-07-0641CrossRefPubMedPubMedCentralGoogle Scholar
  41. Gall JG (1967) Octagonal nuclear pores. J Cell Biol 32:391–399CrossRefPubMedPubMedCentralGoogle Scholar
  42. Grossman E, Medalia O, Zwerger M (2012) Functional architecture of the nuclear pore complex. Annu Rev Biophys 41:557–584.  https://doi.org/10.1146/annurev-biophys-050511-102328CrossRefPubMedGoogle Scholar
  43. Gruenbaum Y, Foisner R (2015) Lamins: nuclear intermediate filament proteins with fundamental functions in nuclear mechanics and genome regulation. Annu Rev Biochem 84:131–164.  https://doi.org/10.1146/annurev-biochem-060614-034115CrossRefPubMedGoogle Scholar
  44. Gustin KE, Sarnow P (2001) Effects of poliovirus infection on nucleo-cytoplasmic trafficking and nuclear pore complex composition. EMBO J 20:240–249.  https://doi.org/10.1093/emboj/20.1.240CrossRefPubMedPubMedCentralGoogle Scholar
  45. Gustin KE, Sarnow P (2002) Inhibition of nuclear import and alteration of nuclear pore complex composition by rhinovirus. J Virol 76:8787–8796.  https://doi.org/10.1128/JVI.76.17.8787-8796.2002CrossRefPubMedPubMedCentralGoogle Scholar
  46. Güttler T, Görlich D (2011) Ran-dependent nuclear export mediators: a structural perspective. EMBO J 30:3457–3474.  https://doi.org/10.1038/emboj.2011.287CrossRefPubMedPubMedCentralGoogle Scholar
  47. Hatch EM, Hetzer MW (2016) Nuclear envelope rupture is induced by actin-based nucleus confinement. J Cell Biol 215(1):5–8.  https://doi.org/10.1083/jcb.201603053CrossRefGoogle Scholar
  48. Hawryluk-Gara LA, Shibuya EK, Wozniak RW (2005) Vertebrate Nup53 interacts with the nuclear lamina and is required for the assembly of a Nup93-containing complex. Mol Biol Cell 16:2382–2394.  https://doi.org/10.1091/mbc.E04-10-0857CrossRefPubMedPubMedCentralGoogle Scholar
  49. Hetzer M, Meyer HH, Walther TC, Bilbao-Cortes D, Warren G, Mattaj IW (2001) Distinct AAA-ATPase p97 complexes function in discrete steps of nuclear assembly. Nat Cell Biol 3:1086–1091.  https://doi.org/10.1038/ncb1201-1086CrossRefPubMedGoogle Scholar
  50. Hinshaw JE, Carragher BO, Milligan RA (1992) Architecture and design of the nuclear pore complex. Cell 69:1133–1141.  https://doi.org/10.1016/0092-8674(92)90635-PCrossRefPubMedGoogle Scholar
  51. Ho CY, Jaalouk DE, Vartiainen MK, Lammerding J (2013) Lamin A/C and emerin regulate MKL1–SRF activity by modulating actin dynamics. Nature 497:507–511.  https://doi.org/10.1038/nature12105CrossRefPubMedPubMedCentralGoogle Scholar
  52. Hodzic DM, Yeater DB, Bengtsson L, Otto H, Stahl PD (2004) Sun2 is a novel mammalian inner nuclear membrane protein. J Biol Chem 279:25805–25812.  https://doi.org/10.1074/jbc.M313157200CrossRefPubMedGoogle Scholar
  53. Holaska JM, Rais-Bahrami S, Wilson KL (2006) Lmo7 is an emerin-binding protein that regulates the transcription of emerin and many other muscle-relevant genes. Hum Mol Genet 15:3459–3472.  https://doi.org/10.1093/hmg/ddl423CrossRefPubMedGoogle Scholar
  54. Ivorra C, Kubicek M, González JM, Sanz-González SM, Alvarez-Barrientos A, O’Connor J-E, Burke B, Andrés V (2006) A mechanism of AP-1 suppression through interaction of c-Fos with lamin A/C. Genes Dev 20:307–320.  https://doi.org/10.1101/gad.349506CrossRefPubMedPubMedCentralGoogle Scholar
  55. Katta SS, Smoyer CJ, Jaspersen SL (2014) Destination: inner nuclear membrane. Trends Cell Biol 24:221–229.  https://doi.org/10.1016/j.tcb.2013.10.006CrossRefPubMedGoogle Scholar
  56. Kennedy BK, Barbie DA, Classon M, Dyson N, Harlow E (2000) Nuclear organization of DNA replication in primary mammalian cells. Genes Dev 14:2855–2868CrossRefPubMedPubMedCentralGoogle Scholar
  57. Kerr AR, Schirmer EC (2011) FG repeats facilitate integral protein trafficking to the inner nuclear membrane. Commun Integr Biol 4:557–559.  https://doi.org/10.4161/cib.4.5.16052CrossRefPubMedPubMedCentralGoogle Scholar
  58. Kill IR, Hutchison CJ (1995) S-Phase phosphorylation of lamin B2. FEBS Lett 377:26–30.  https://doi.org/10.1016/0014-5793(95)01302-4CrossRefPubMedGoogle Scholar
  59. King MC, Lusk CP, Blobel G (2006) Karyopherin-mediated import of integral inner nuclear membrane proteins. Nature 442:1003–1007.  https://doi.org/10.1038/nature05075CrossRefPubMedGoogle Scholar
  60. Knockenhauer KE, Schwartz TU (2016) The nuclear pore complex as a flexible and dynamic gate. Cell 164:1162–1171.  https://doi.org/10.1016/j.cell.2016.01.034CrossRefPubMedPubMedCentralGoogle Scholar
  61. Kobe B (1999) Autoinhibition by an internal nuclear localization signal revealed by the crystal structure of mammalian importin α. Nat Struct Biol 6:388–397.  https://doi.org/10.1038/7625CrossRefPubMedGoogle Scholar
  62. Korfali N, Wilkie GS, Swanson SK, Srsen V, Batrakou DG, Fairley EAL, Malik P, Zuleger N, Goncharevich A, de Las Heras J, Kelly DA, Kerr ARW, Florens L, Schirmer EC (2010) The leukocyte nuclear envelope proteome varies with cell activation and contains novel transmembrane proteins that affect genome architecture. Mol Cell Proteomics 9:2571–2585.  https://doi.org/10.1074/mcp.M110.002915CrossRefPubMedPubMedCentralGoogle Scholar
  63. Korfali N, Wilkie GS, Swanson SK, Srsen V, de las Heras J, Batrakou DG, Malik P, Zuleger N, Kerr ARW, Florens L, Schirmer EC (2012) The nuclear envelope proteome differs notably between tissues. Nucleus 3:552–564.  https://doi.org/10.4161/nucl.22257CrossRefPubMedPubMedCentralGoogle Scholar
  64. Kosinski J, Mosalaganti S, von Appen A, Teimer R, Diguilio AL, Wan W, Bui KH, Hagen WJH, Briggs JAG, Glavy JS, Hurt E, Beck M (2016) Molecular architecture of the inner ring scaffold of the human nuclear pore complex. Science 352:363–366CrossRefPubMedGoogle Scholar
  65. Kralt A, Jagalur NB, van den Boom V, Lokareddy RK, Steen A, Cingolani G, Fornerod M, Veenhoff LM (2015) Conservation of inner nuclear membrane targeting sequences in mammalian Pom121 and yeast Heh2 membrane proteins. Mol Biol Cell 26:3301–3312.  https://doi.org/10.1091/mbc.E15-03-0184CrossRefPubMedPubMedCentralGoogle Scholar
  66. Laba J, Steen A, Popken P, Chernova A, Poolman B, Veenhoff L (2015) Active nuclear import of membrane proteins revisited. Cells 4:653–673.  https://doi.org/10.3390/cells4040653CrossRefPubMedPubMedCentralGoogle Scholar
  67. Laba JK, Steen A, Veenhoff LM (2014) Traffic to the inner membrane of the nuclear envelope. Curr Opin Cell Biol 28:36–45.  https://doi.org/10.1016/j.ceb.2014.01.006CrossRefPubMedGoogle Scholar
  68. Lammerding J, Fong LG, Ji JY, Reue K, Stewart CL, Young SG, Lee RT (2006) Lamins A and C but not lamin B1 regulate nuclear mechanics. J Biol Chem 281:25768–25780.  https://doi.org/10.1074/jbc.M513511200CrossRefPubMedGoogle Scholar
  69. Lammerding J, Schulze PC, Takahashi T, Kozlov S, Sullivan T, Kamm RD, Stewart CL, Lee RT (2004) Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J Clin Invest 113:370–378.  https://doi.org/10.1172/JCI19670CrossRefPubMedPubMedCentralGoogle Scholar
  70. Leach NR, Roller RJ (2010) Significance of host cell kinases in herpes simplex virus type 1 egress and lamin-associated protein disassembly from the nuclear lamina. Virology 406:127–137.  https://doi.org/10.1016/j.virol.2010.07.002CrossRefPubMedPubMedCentralGoogle Scholar
  71. Lee JSH, Hale CM, Panorchan P, Khatau SB, George JP, Tseng Y, Stewart CL, Hodzic D, Wirtz D (2007) Nuclear lamin A/C deficiency induces defects in cell mechanics, polarization, and migration. Biophys J 93:2542–2552.  https://doi.org/10.1529/biophysj.106.102426CrossRefPubMedPubMedCentralGoogle Scholar
  72. Levin JM, Robson B, Garnier J (1986) An algorithm for secondary structure determination in proteins based on sequence similarity. FEBS Lett 205:303–308.  https://doi.org/10.1016/0014-5793(86)80917-6CrossRefPubMedGoogle Scholar
  73. Lill Y, M a L, Fahrenkrog B, Schwarz-Herion K, Paulillo S, Aebi U, Hecht B (2006) Single hepatitis-B virus core capsid binding to individual nuclear pore complexes in Hela cells. Biophys J 91:3123–3130.  https://doi.org/10.1529/biophysj.106.087650CrossRefPubMedPubMedCentralGoogle Scholar
  74. Liu D, Wu X, Summers MD, Lee A, Ryan KJ, Braunagel SC (2010) Truncated isoforms of Kap60 facilitate trafficking of Heh2 to the nuclear envelope. Traffic 11:1506–1518.  https://doi.org/10.1111/j.1600-0854.2010.01119.xCrossRefPubMedGoogle Scholar
  75. Lusk CP, Blobel G, King MC (2007) Highway to the inner nuclear membrane: rules for the road. Nat Rev Mol Cell Biol 8:414–420.  https://doi.org/10.1038/nrm2165CrossRefPubMedGoogle Scholar
  76. Ma Y, Cai S, Lv Q, Jiang Q, Zhang Q, Sodmergen, Zhai Z, Zhang C (2007) Lamin B receptor plays a role in stimulating nuclear envelope production and targeting membrane vesicles to chromatin during nuclear envelope assembly through direct interaction with importin beta. J Cell Sci 120:520–530.  https://doi.org/10.1242/jcs.03355CrossRefPubMedGoogle Scholar
  77. Maeshima K, Iino H, Hihara S, Imamoto N (2011) Nuclear size, nuclear pore number and cell cycle. Nucleus 1034:1–6.  https://doi.org/10.1038/nsmb.1878.nCrossRefGoogle Scholar
  78. Maimon T, Elad N, Dahan I, Medalia O (2012) The human nuclear pore complex as revealed by cryo-electron tomography. Structure 20:998–1006.  https://doi.org/10.1016/j.str.2012.03.025CrossRefPubMedGoogle Scholar
  79. Makarova M, Oliferenko S (2016) Mixing and matching nuclear envelope remodeling and spindle assembly strategies in the evolution of mitosis. Curr Opin Cell Biol 41:43–50.  https://doi.org/10.1016/j.ceb.2016.03.016CrossRefPubMedGoogle Scholar
  80. Makatsori D, Kourmouli N, Polioudaki H, Shultz LD, McLean K, Theodoropoulos PA, Singh PB, Georgatos SD (2004) The inner nuclear membrane protein lamin B receptor forms distinct microdomains and links epigenetically marked chromatin to the nuclear envelope. J Biol Chem 279:25567–25573.  https://doi.org/10.1074/jbc.M313606200CrossRefPubMedGoogle Scholar
  81. Malik P, Korfali N, Vlastimil S, Lazou V, Dzmitry B, Nikolaj Z, Kavanagh DM, Wilkie GS, Goldberg MW, Schirmer EC (2010) Cell-specific and lamin-dependent targeting of novel transmembrane proteins in the nuclear envelope. Cell Mol Life Sci 67:1353–1369.  https://doi.org/10.1007/s00018-010-0257-2CrossRefPubMedPubMedCentralGoogle Scholar
  82. Malik P, Zuleger N, de las Heras JI, Saiz-Ros N, Makarov AA, Lazou V, Meinke P, Waterfall M, Kelly DA, Schirmer EC (2014) NET23/STING promotes chromatin compaction from the nuclear envelope. PLoS One 9(11):e111851.  https://doi.org/10.1371/journal.pone.0111851CrossRefPubMedPubMedCentralGoogle Scholar
  83. Markiewicz E, Dechat T, Foisner R, Quinlan RA, Hutchison CJ (2002) Lamin A/C binding protein LAP2alpha is required for nuclear anchorage of retinoblastoma protein. Mol Biol Cell 13:4401–4413.  https://doi.org/10.1091/mbc.E02-07-0450CrossRefPubMedPubMedCentralGoogle Scholar
  84. Maul GG (1972) Time sequence of nuclear pore formation in phytohemagglutinin-stimulated lymphocytes and in hela cells during the cell cycle. J Cell Biol 55:433–447.  https://doi.org/10.1083/jcb.55.2.433CrossRefPubMedPubMedCentralGoogle Scholar
  85. Meaburn KJ, Cabuy E, Bonne G, Levy N, Morris GE, Novelli G, Kill IR, Bridger JM (2007) Primary laminopathy fibroblasts display altered genome organization and apoptosis. Aging Cell 6:139–153.  https://doi.org/10.1111/j.1474-9726.2007.00270.xCrossRefPubMedGoogle Scholar
  86. Meier J, Campbell KH, Ford CC, Stick R, Hutchison CJ (1991) The role of lamin LIII in nuclear assembly and DNA replication, in cell-free extracts of Xenopus eggs. J Cell Sci 98(Pt 3):271–279PubMedGoogle Scholar
  87. Meinema AC, Laba JK, Hapsari RA, Otten R, Mulder FAA, Kralt A, van den Bogaart G, Lusk CP, Poolman B, Veenhoff LM (2011) Long unfolded linkers facilitate membrane protein import through the nuclear pore complex. Science 333:90–93.  https://doi.org/10.1126/science.1205741CrossRefPubMedGoogle Scholar
  88. Meinema AC, Poolman B, Veenhoff LM (2013) Quantitative analysis of membrane protein transport across the nuclear pore complex. Traffic 14:487–501.  https://doi.org/10.1111/tra.12048CrossRefPubMedGoogle Scholar
  89. Melcák I, Hoelz A, Blobel G (2007) Structure of Nup58/45 suggests flexible nuclear pore diameter by intermolecular sliding. Science 315:1729–1732.  https://doi.org/10.1126/science.1135730CrossRefPubMedGoogle Scholar
  90. Mészáros N, Cibulka J, Mendiburo MJ, Romanauska A, Schneider M, Köhler A (2015) Nuclear pore basket proteins are tethered to the nuclear envelope and can regulate membrane curvature. Dev Cell 33:285–298.  https://doi.org/10.1016/j.devcel.2015.02.017CrossRefPubMedPubMedCentralGoogle Scholar
  91. Mettenleiter TC, Müller F, Granzow H, Klupp BG (2013) The way out: what we know and do not know about herpesvirus nuclear egress. Cell Microbiol 15:170–178.  https://doi.org/10.1111/cmi.12044CrossRefPubMedGoogle Scholar
  92. Mewborn SK, Puckelwartz MJ, Abuisneineh F, Fahrenbach JP, Zhang Y, MacLeod H, Dellefave L, Pytel P, Selig S, Labno CM, Reddy K, Singh H, McNally E (2010) Altered chromosomal positioning, compaction, and gene expression with a lamin A/C gene mutation. PLoS One 5:e14342.  https://doi.org/10.1371/journal.pone.0014342CrossRefPubMedPubMedCentralGoogle Scholar
  93. Milbradt J, Auerochs S, Marschall M (2007) Cytomegaloviral proteins pUL50 and pUL53 are associated with the nuclear lamina and interact with cellular protein kinase C. J Gen Virol 88:2642–2650.  https://doi.org/10.1099/vir.0.82924-0CrossRefPubMedGoogle Scholar
  94. Milbradt J, Auerochs S, Sticht H, Marschall M (2009) Cytomegaloviral proteins that associate with the nuclear lamina: components of a postulated nuclear egress complex. J Gen Virol 90:579–590.  https://doi.org/10.1099/vir.0.005231-0CrossRefPubMedGoogle Scholar
  95. Moir RD, Montag-Lowy M, Goldman RD (1994) Dynamic properties of nuclear lamins: lamin B is associated with sites of DNA replication. J Cell Biol 125:1201–1212CrossRefPubMedGoogle Scholar
  96. Muranyi W, Haas J, Wagner M, Krohne G, Koszinowski UH (2002) Cytomegalovirus recruitment of cellular kinases to dissolve the nuclear lamina. Science 297:854–857.  https://doi.org/10.1126/science.1071506CrossRefPubMedGoogle Scholar
  97. Nakai K, Horton P (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24:34–35.  https://doi.org/10.1016/S0968-0004(98)01336-XCrossRefPubMedGoogle Scholar
  98. Nili E, Cojocaru GS, Kalma Y, Ginsberg D, Copeland NG, Gilbert DJ, Jenkins NA, Berger R, Shaklai S, Amariglio N, Brok-Simoni F, Simon a J, Rechavi G (2001) Nuclear membrane protein LAP2β mediates transcriptional repression alone and together with its binding partner GCL (germ-cell-less). J Cell Sci 114:3297–3307.  https://doi.org/10.1111/j.1600-0447.1959.tb07559.xCrossRefPubMedGoogle Scholar
  99. Ohba T, Schirmer EC, Nishimoto T, Gerace L (2004) Energy- and temperature-dependent transport of integral proteins to the inner nuclear membrane via the nuclear pore. J Cell Biol 167:1051–1062.  https://doi.org/10.1083/jcb.200409149CrossRefPubMedPubMedCentralGoogle Scholar
  100. Olmos Y, Hodgson L, Mantell J, Verkade P, Carlton JG (2015) ESCRT-III controls nuclear envelope reformation. Nature 522:236–239.  https://doi.org/10.1038/nature14503CrossRefPubMedPubMedCentralGoogle Scholar
  101. Östlund C, Ellenberg J, Hallberg E, Lippincott-Schwartz J, Worman HJ (1999) Intracellular trafficking of emerin, the Emery-Dreifuss muscular dystrophy protein. J Cell Sci 112:1709–1719PubMedGoogle Scholar
  102. Östlund C, Sullivan T, Stewart CL, Worman HJ (2006) Dependence of diffusional mobility of integral inner nuclear membrane proteins on A-type lamins. Biochemistry 45:1374–1382.  https://doi.org/10.1021/bi052156nCrossRefPubMedPubMedCentralGoogle Scholar
  103. Ottaviano Y, Gerace L (1985) Phosphorylation of the nuclear lamins during interphase and mitosis. J Biol Chem 260:624–632PubMedGoogle Scholar
  104. Pante N, Kann M (2002) Nuclear pore complex is able to transport macromolecules with diameters of 39 nm. Mol Biol Cell 13:425–434.  https://doi.org/10.1091/mbc01CrossRefPubMedPubMedCentralGoogle Scholar
  105. Pekovic V, Harborth J, Broers JLV, Ramaekers FCS, van Engelen B, Lammens M, von Zglinicki T, Foisner R, Hutchison C, Markiewicz E (2007) Nucleoplasmic LAP2α–lamin A complexes are required to maintain a proliferative state in human fibroblasts. J Cell Biol 176:163–172.  https://doi.org/10.1083/jcb.200606139CrossRefPubMedPubMedCentralGoogle Scholar
  106. Powell L, Burke B (1990) Internuclear exchange of an inner nuclear membrane protein (p55) in heterokaryons: In vivo evidence for the interaction of p55 with the nuclear lamina. J Cell Biol 111:2225–2234.  https://doi.org/10.1083/jcb.111.6.2225CrossRefPubMedGoogle Scholar
  107. Rabut G, Doye V, Ellenberg J (2004) Mapping the dynamic organization of the nuclear pore complex inside single living cells. Nat Cell Biol 6:1114–1121.  https://doi.org/10.1038/ncb1184CrossRefPubMedGoogle Scholar
  108. Reichelt R, Holzenburg A, Buhle EL, Engel A (1990) Correlation between structure and mass distribution of the nuclear pore complex and of distinct pore complex components. J Cell Biol 110:883–894CrossRefPubMedGoogle Scholar
  109. Rexach M, Blobel G (1995) Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 83:683–692.  https://doi.org/10.1016/0092-8674(95)90181-7CrossRefPubMedGoogle Scholar
  110. Rexach MF (2006) A sorting importin on Sec61. Nat Struct Mol Biol 13:476–478.  https://doi.org/10.1038/nsmb0606-476CrossRefPubMedGoogle Scholar
  111. Robson MI, de las Heras JI, Czapiewski R, Lê Thành P, Booth DG, Kelly DA, Webb S, Kerr ARW, Schirmer EC (2016) Tissue-specific gene repositioning by muscle nuclear membrane proteins enhances repression of critical developmental genes during myogenesis. Mol Cell 62:834–847.  https://doi.org/10.1016/j.molcel.2016.04.035CrossRefPubMedPubMedCentralGoogle Scholar
  112. Rounsevell R, Forman JR, Clarke J (2004) Atomic force microscopy: mechanical unfolding of proteins. Methods 34:100–111.  https://doi.org/10.1016/j.ymeth.2004.03.007CrossRefPubMedGoogle Scholar
  113. Rout MP, Aitchison JD, Suprapto A, Hjertaas K, Zhao Y, Chait BT (2000) The yeast nuclear pore complex. J Cell Biol 148:635–652.  https://doi.org/10.1083/jcb.148.4.635CrossRefPubMedPubMedCentralGoogle Scholar
  114. Saksena S, Shao Y, Braunagel SC, Summers MD, Johnson AE (2004) Cotranslational integration and initial sorting at the endoplasmic reticulum translocon of proteins destined for the inner nuclear membrane. Proc Natl Acad Sci USA 101:12537–12542.  https://doi.org/10.1073/pnas.0404934101CrossRefPubMedGoogle Scholar
  115. Saksena S, Summers MD, Burks JK, Johnson AE, Braunagel SC (2006) Importin-alpha-16 is a translocon-associated protein involved in sorting membrane proteins to the nuclear envelope. Nat Struct Mol Biol 13:500–508.  https://doi.org/10.1038/nsmb1098CrossRefPubMedGoogle Scholar
  116. Schirmer EC, Florens L, Guan T, Yates JR, Gerace L (2003) Nuclear membrane proteins with potential disease links found by subtractive proteomics. Science 301:1380–1382.  https://doi.org/10.1126/science.1088176CrossRefPubMedGoogle Scholar
  117. Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M (2011) Global quantification of mammalian gene expression control. Nature 473:337–342.  https://doi.org/10.1038/nature11848CrossRefPubMedGoogle Scholar
  118. Senior A, Gerace L (1988) Integral membrane proteins specific to the inner nuclear membrane and associated with the nuclear lamina. J Cell Biol 107:2029–2036.  https://doi.org/10.1083/JCB.107.6.2029CrossRefPubMedGoogle Scholar
  119. Shaklai S, Amariglio N, Rechavi G, Simon AJ (2007) Gene silencing at the nuclear periphery. FEBS J 274:1383–1392.  https://doi.org/10.1111/j.1742-4658.2007.05697.xCrossRefPubMedGoogle Scholar
  120. Sharma A, Solmaz SR, Blobel G, Melčák I (2015) Ordered regions of channel nucleoporins Nup62, Nup54, and Nup58 form dynamic complexes in solution. J Biol Chem 290:18370–18378.  https://doi.org/10.1074/jbc.M115.663500CrossRefPubMedPubMedCentralGoogle Scholar
  121. Shimi T, Butin-Israeli V, Adam SA, Hamanaka RB, Goldman AE, Lucas CA, Shumaker DK, Kosak ST, Chandel NS, Goldman RD (2011) The role of nuclear lamin B1 in cell proliferation and senescence. Genes Dev 25:2579–2593.  https://doi.org/10.1101/gad.179515.111CrossRefPubMedPubMedCentralGoogle Scholar
  122. Shimi T, Koujin T, Segura-Totten M, Wilson KL, Haraguchi T, Hiraoka Y (2004) Dynamic interaction between BAF and emerin revealed by FRAP, FLIP, and FRET analyses in living HeLa cells. J Struct Biol 147:31–41.  https://doi.org/10.1016/j.jsb.2003.11.013CrossRefPubMedGoogle Scholar
  123. Smith S, Blobel G (1993) The first membrane spanning region of the lamin B receptor is sufficient for sorting to the inner nuclear membrane. J Cell Biol 120:631–637.  https://doi.org/10.1083/jcb.120.3.631CrossRefPubMedGoogle Scholar
  124. Smoyer CJ, Jaspersen SL (2014) Breaking down the wall: the nuclear envelope during mitosis. Curr Opin Cell Biol 26:1–9.  https://doi.org/10.1016/j.ceb.2013.08.002CrossRefPubMedGoogle Scholar
  125. Smythe C, Jenkins HE, Hutchison CJ (2000) Incorporation of the nuclear pore basket protein Nup153 into nuclear pore structures is dependent upon lamina assembly: evidence from cell-free extracts of Xenopus eggs. EMBO J 19:3918–3931.  https://doi.org/10.1093/emboj/19.15.3918CrossRefPubMedPubMedCentralGoogle Scholar
  126. Solmaz SR, Blobel G, Melcák I (2013) Ring cycle for dilating and constricting the nuclear pore. Proc Natl Acad Sci USA 110:5858–5863.  https://doi.org/10.1073/pnas.1302655110CrossRefPubMedGoogle Scholar
  127. Soullam B, Worman HJ (1995) Signals and structural features involved in integral membrane protein targeting to the inner nuclear membrane. J Cell Biol 130:15–27.  https://doi.org/10.1083/jcb.130.1.15CrossRefPubMedGoogle Scholar
  128. Soullam B, Worman HJ (1993) The amino-terminal domain of the lamin B receptor is a nuclear envelope targeting signal. J Cell Biol 120:1093–1100CrossRefPubMedGoogle Scholar
  129. Spann TP, Moir RD, Goldman AE, Stick R, Goldman RD (1997) Disruption of nuclear lamin organization alters the distribution of replication factors and inhibits DNA synthesis. J Cell Biol 136:1201–1212CrossRefPubMedPubMedCentralGoogle Scholar
  130. Speese SD, Ashley J, Jokhi V, Nunnari J, Barria R, Li Y, Ataman B, Koon A, Chang YT, Li Q, Moore MJ, Budnik V (2012) Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling. Cell 149:832–846.  https://doi.org/10.1016/j.cell.2012.03.032CrossRefPubMedPubMedCentralGoogle Scholar
  131. Swift J, Ivanovska IL, Buxboim A, Harada T, Dingal PCDP, Pinter J, Pajerowski JD, Spinler KR, Shin J-W, Tewari M, Rehfeldt F, Speicher DW, Discher DE (2013) Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 341:1240104–1240104.  https://doi.org/10.1126/science.1240104CrossRefPubMedPubMedCentralGoogle Scholar
  132. Terry LJ, Wente SR (2009) Flexible gates: dynamic topologies and functions for FG nucleoporins in nucleocytoplasmic transport. Eukaryot Cell 8:1814–1827.  https://doi.org/10.1128/EC.00225-09CrossRefPubMedPubMedCentralGoogle Scholar
  133. Theerthagiri G, Eisenhardt N, Schwarz H, Antonin W (2010) The nucleoporin Nup188 controls passage of membrane proteins across the nuclear pore complex. J Cell Biol 189:1129–1142.  https://doi.org/10.1083/jcb.200912045CrossRefPubMedPubMedCentralGoogle Scholar
  134. Torrisi MR, Lotti LV, Pavan A, Migliaccio G, Bonatti S (1987) Free diffusion to and from the inner nuclear membrane of newly synthesized plasma membrane glycoproteins. J Cell Biol 104:733–737CrossRefPubMedGoogle Scholar
  135. Turgay Y, Ungricht R, Rothballer A, Kiss A, Csucs G, Horvath P, Kutay U (2010) A classical NLS and the SUN domain contribute to the targeting of SUN2 to the inner nuclear membrane. EMBO J 29:2262–2275.  https://doi.org/10.1038/emboj.2010.119CrossRefPubMedPubMedCentralGoogle Scholar
  136. Ulbert S, Platani M, Boue S, Mattaj IW (2006) Direct membrane protein–DNA interactions required early in nuclear envelope assembly. J Cell Biol 173:469–476.  https://doi.org/10.1083/jcb.200512078CrossRefPubMedPubMedCentralGoogle Scholar
  137. Ungricht R, Klann M, Horvath P, Kutay U (2015) Diffusion and retention are major determinants of protein targeting to the inner nuclear membrane. J Cell Biol 209:687–704.  https://doi.org/10.1083/jcb.201409127CrossRefPubMedPubMedCentralGoogle Scholar
  138. Ungricht R, Kutay U (2015) Establishment of NE asymmetry—targeting of membrane proteins to the inner nuclear membrane. Curr Opin Cell Biol 34:135–141.  https://doi.org/10.1016/j.ceb.2015.04.005CrossRefPubMedGoogle Scholar
  139. Unwin PNT, Milligan RA (1982) A large particle associated with the perimeter of the nuclear pore complex. J Cell Biol 93:63–75CrossRefPubMedGoogle Scholar
  140. Vargas JD, Hatch EM, Anderson DJ, Hetzer MW (2012) Transient nuclear envelope rupturing during interphase in human cancer cells. Nucleus 3:88–100.  https://doi.org/10.4161/nucl.18954CrossRefPubMedPubMedCentralGoogle Scholar
  141. von Appen A, Beck M (2016) Structure determination of the nuclear pore complex with three-dimensional cryo electron microscopy. J Mol Biol 428:2001–2010.  https://doi.org/10.1016/j.jmb.2016.01.004CrossRefGoogle Scholar
  142. von Appen A, Kosinski J, Sparks L, Ori A, DiGuilio AL, Vollmer B, Mackmull M-T, Banterle N, Parca L, Kastritis P, Buczak K, Mosalaganti S, Hagen W, Andres-Pons A, Lemke EA, Bork P, Antonin W, Glavy JS, Bui KH, Beck M (2015) In situ structural analysis of the human nuclear pore complex. Nature 526:140–143.  https://doi.org/10.1038/nature15381CrossRefGoogle Scholar
  143. Wilkie GS, Korfali N, Swanson SK, Malik P, Srsen V, Batrakou DG, de las Heras J, Zuleger N, Kerr ARW, Florens L, Schirmer EC (2011) Several novel nuclear envelope transmembrane proteins identified in skeletal muscle have cytoskeletal associations. Mol Cell Proteomics 10:M110.003129.  https://doi.org/10.1074/mcp.M110.003129CrossRefPubMedGoogle Scholar
  144. Willis ND, Cox TR, Rahman-Casañs SF, Smits K, Przyborski SA, van den Brandt P, van Engeland M, Weijenberg M, Wilson RG, de Bruïne A, Hutchison CJ (2008) Lamin A/C is a risk biomarker in colorectal cancer. PLoS One 3:e2988.  https://doi.org/10.1371/journal.pone.0002988CrossRefPubMedPubMedCentralGoogle Scholar
  145. Worman HJ, Schirmer EC (2015) Nuclear membrane diversity: underlying tissue-specific pathologies in disease? Curr Opin Cell Biol 34:101–112.  https://doi.org/10.1016/j.ceb.2015.06.003CrossRefPubMedPubMedCentralGoogle Scholar
  146. Worman HJ, Yuan J, Blobel G, Georgatos SD (1988) A lamin B receptor in the nuclear envelope. Proc Natl Acad Sci USA 85:8531–8534CrossRefPubMedGoogle Scholar
  147. Wu W, Lin F, Worman HJ (2002) Intracellular trafficking of MAN1, an integral protein of the nuclear envelope inner membrane. J Cell Sci 115:1361–1371PubMedGoogle Scholar
  148. Yang W (2013) Distinct, but not completely separate spatial transport routes in the nuclear pore complex. Nucleus 4:166–175.  https://doi.org/10.4161/nucl.24874CrossRefPubMedPubMedCentralGoogle Scholar
  149. Ye Q, Worman HJ (1996) Interaction between an integral protein of the nuclear envelope inner membrane and human chromodomain proteins homologous to Drosophila HP1. J Biol Chem 271:14653–14656.  https://doi.org/10.1074/JBC.271.25.14653CrossRefPubMedGoogle Scholar
  150. Ye Q, Worman HJ (1994) Primary structure analysis and lamin B and DNA binding of human LBR, an integral protein of the nuclear envelope inner membrane. J Biol Chem 269:11306–11311PubMedGoogle Scholar
  151. Zuleger N, Boyle S, Kelly DA, de las Heras JI, Lazou V, Korfali N, Batrakou DG, Randles KN, Morris GE, Harrison DJ, Bickmore WA, Schirmer EC (2013) Specific nuclear envelope transmembrane proteins can promote the location of chromosomes to and from the nuclear periphery. Genome Biol 14:R14.  https://doi.org/10.1186/gb-2013-14-2-r14CrossRefPubMedPubMedCentralGoogle Scholar
  152. Zuleger N, Kelly DA, Richardson AC, Kerr ARW, Goldberg MW, Goryachev AB, Schirmer EC (2011) System analysis shows distinct mechanisms and common principles of nuclear envelope protein dynamics. J Cell Biol 193:109–123.  https://doi.org/10.1083/jcb.201009068CrossRefPubMedPubMedCentralGoogle Scholar
  153. Zuleger N, Kerr ARW, Schirmer EC (2012) Many mechanisms, one entrance: membrane protein translocation into the nucleus. Cell Mol Life Sci 69:2205–2216.  https://doi.org/10.1007/s00018-012-0929-1CrossRefPubMedGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.The Wellcome Trust Centre for Cell BiologyUniversity of EdinburghEdinburghUK

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