Advertisement

Non-canonical Roles of Nuclear Pore Proteins

  • Douglas R. Mackay
  • Katharine S. Ullman
Chapter
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 33)

Abstract

Thousands of nuclear pore complexes stud the nuclear envelope of a proliferating mammalian cell. At these sites, ∼30 proteins, each present in multiple copies, come together to provide a selective trafficking gateway. In addition to this vital canonical role in nucleocytoplasmic trafficking, a wide variety of other important biological functions are carried out by nuclear pore proteins. In this chapter, we survey the broad range of noncanonical roles that nuclear pore proteins play beyond the nuclear pore complex: during mitosis, in the regulation of gene expression, in response to DNA damage, at primary cilia, and as a signaling or tethering platform for other cellular processes. This chapter provides a snapshot of the scientific literature that emphasizes an ever-growing appreciation of the diverse contributions that nuclear pore proteins make to cell biology. This broader context is particularly important when considering experimental and disease-related phenotypes that arise when the role of a nuclear pore protein is impaired. An appreciation of non-canonical roles also underscores the potential for regulatory cross-talk between the status of nucleocytoplasmic trafficking and other cell functions.

References

  1. Adams RL, Wente SR (2013) Uncovering nuclear pore complexity with innovation. Cell 152:1218–1221PubMedPubMedCentralCrossRefGoogle Scholar
  2. Bai XT, Gu BW, Yin T, Niu C, Xi XD, Zhang J, Chen Z, Chen SJ (2006) Trans-repressive effect of NUP98-PMX1 on PMX1-regulated c-FOS gene through recruitment of histone deacetylase 1 by FG repeats. Cancer Res 66:4584–4590PubMedCrossRefGoogle Scholar
  3. Beaudouin J, Gerlich D, Daigle N, Eils R, Ellenberg J (2002) Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina. Cell 108:83–96PubMedCrossRefGoogle Scholar
  4. Belgareh N, Rabut G, Bai SW, Van Overbeek M, Beaudouin J, Daigle N, Zatsepina OV, Pasteau F, Labas V, Fromont-Racine M, Ellenberg J, Doye V (2001) An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells. J Cell Biol 154:1147–1160PubMedPubMedCentralCrossRefGoogle Scholar
  5. Bolhy S, Bouhlel I, Dultz E, Nayak T, Zuccolo M, Gatti X, Vallee R, Ellenberg J, Doye V (2011) A Nup133-dependent NPC-anchored network tethers centrosomes to the nuclear envelope in prophase. J Cell Biol 192:855–871PubMedPubMedCentralCrossRefGoogle Scholar
  6. Breslow DK, Koslover EF, Seydel F, Spakowitz AJ, Nachury MV (2013) An in vitro assay for entry into cilia reveals unique properties of the soluble diffusion barrier. J Cell Biol 203:129–147PubMedPubMedCentralCrossRefGoogle Scholar
  7. Brown CR, Kennedy CJ, Delmar VA, Forbes DJ, Silver PA (2008) Global histone acetylation induces functional genomic reorganization at mammalian nuclear pore complexes. Genes Dev 22:627–639PubMedPubMedCentralCrossRefGoogle Scholar
  8. Buchwalter AL, Liang Y, Hetzer MW (2014) Nup50 is required for cell differentiation and exhibits transcription-dependent dynamics. Mol Biol Cell 25:2472–2484PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bui KH, Von Appen A, Diguilio AL, Ori A, Sparks L, Mackmull MT, Bock T, Hagen W, Andres-Pons A, Glavy JS, Beck M (2013) Integrated structural analysis of the human nuclear pore complex scaffold. Cell 155:1233–1243PubMedCrossRefGoogle Scholar
  10. Capelson M, Liang Y, Schulte R, Mair W, Wagner U, Hetzer MW (2010) Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell 140:372–383PubMedPubMedCentralCrossRefGoogle Scholar
  11. Capitanio JS, Montpetit B, Wozniak RW (2017) Human Nup98 regulates the localization and activity of DExH/D-box helicase DHX9. Elife 6:e18825PubMedPubMedCentralCrossRefGoogle Scholar
  12. Carvalhal S, Ribeiro SA, Arocena M, Kasciukovic T, Temme A, Koehler K, Huebner A, Griffis ER (2015) The nucleoporin ALADIN regulates Aurora A localization to ensure robust mitotic spindle formation. Mol Biol Cell 26:3424–3438PubMedPubMedCentralCrossRefGoogle Scholar
  13. Ceccaldi R, Rondinelli B, D’Andrea AD (2016) Repair pathway choices and consequences at the double-strand break. Trends Cell Biol 26:52–64PubMedCrossRefGoogle Scholar
  14. Chen X, Wang Y, Chen YZ, Harry BL, Nakagawa A, Lee ES, Guo H, Xue D (2016) Regulation of CED-3 caspase localization and activation by C. elegans nuclear-membrane protein NPP-14. Nat Struct Mol Biol 23:958–964PubMedPubMedCentralCrossRefGoogle Scholar
  15. Chow KH, Elgort S, Dasso M, Ullman KS (2012) Two distinct sites in Nup153 mediate interaction with the SUMO proteases SENP1 and SENP2. Nucleus 3:349–358PubMedPubMedCentralCrossRefGoogle Scholar
  16. Chung DK, Chan JN, Strecker J, Zhang W, Ebrahimi-Ardebili S, Lu T, Abraham KJ, Durocher D, Mekhail K (2015) Perinuclear tethers license telomeric DSBs for a broad kinesin- and NPC-dependent DNA repair process. Nat Commun 6:7742PubMedCrossRefGoogle Scholar
  17. Cronshaw JM, Krutchinsky AN, Zhang W, Chait BT, Matunis MJ (2002) Proteomic analysis of the mammalian nuclear pore complex. J Cell Biol 158:915–927PubMedPubMedCentralCrossRefGoogle Scholar
  18. Cross MK, Powers MA (2011) Nup98 regulates bipolar spindle assembly through association with microtubules and opposition of MCAK. Mol Biol Cell 22:661–672PubMedPubMedCentralCrossRefGoogle Scholar
  19. D’Angelo MA, Gomez-Cavazos JS, Mei A, Lackner DH, Hetzer MW (2012) A change in nuclear pore complex composition regulates cell differentiation. Dev Cell 22:446–458PubMedPubMedCentralCrossRefGoogle Scholar
  20. Daigle N, Beaudouin J, Hartnell L, Imreh G, Hallberg E, Lippincott-Schwartz J, Ellenberg J (2001) Nuclear pore complexes form immobile networks and have a very low turnover in live mammalian cells. J Cell Biol 154:71–84PubMedPubMedCentralCrossRefGoogle Scholar
  21. Dawlaty MM, Malureanu L, Jeganathan KB, Kao E, Sustmann C, Tahk S, Shuai K, Grosschedl R, Van Deursen JM (2008) Resolution of sister centromeres requires RanBP2-mediated SUMOylation of topoisomerase IIalpha. Cell 133:103–115PubMedPubMedCentralCrossRefGoogle Scholar
  22. De Castro IJ, Budzak J, Di Giacinto ML, Ligammari L, Gokhan E, Spanos C, Moralli D, Richardson C, De Las Heras JI, Salatino S, Schirmer EC, Ullman KS, Bickmore WA, Green C, Rappsilber J, Lamble S, Goldberg MW, Vinciotti V, Vagnarelli P (2017) Repo-Man/PP1 regulates heterochromatin formation in interphase. Nat Commun 8:14048PubMedPubMedCentralCrossRefGoogle Scholar
  23. Del Viso F, Huang F, Myers J, Chalfant M, Zhang Y, Reza N, Bewersdorf J, Lusk CP, Khokha MK (2016) Congenital heart disease genetics uncovers context-dependent organization and function of nucleoporins at cilia. Dev Cell 38:478–492PubMedPubMedCentralCrossRefGoogle Scholar
  24. Eibauer M, Pellanda M, Turgay Y, Dubrovsky A, Wild A, Medalia O (2015) Structure and gating of the nuclear pore complex. Nat Commun 6:7532PubMedPubMedCentralCrossRefGoogle Scholar
  25. Fernandez-Alvarez A, Cooper JP (2017) Chromosomes orchestrate their own liberation: nuclear envelope disassembly. Trends Cell Biol 27:255–265PubMedCrossRefGoogle Scholar
  26. Franks TM, Hetzer MW (2013) The role of Nup98 in transcription regulation in healthy and diseased cells. Trends Cell Biol 23:112–117PubMedCrossRefGoogle Scholar
  27. Franks TM, Benner C, Narvaiza I, Marchetto MC, Young JM, Malik HS, Gage FH, Hetzer MW (2016) Evolution of a transcriptional regulator from a transmembrane nucleoporin. Genes Dev 30:1155–1171PubMedPubMedCentralGoogle Scholar
  28. Gao N, Davuluri G, Gong W, Seiler C, Lorent K, Furth EE, Kaestner KH, Pack M (2011) The nuclear pore complex protein Elys is required for genome stability in mouse intestinal epithelial progenitor cells. Gastroenterology 140:1547–1555.e10PubMedPubMedCentralCrossRefGoogle Scholar
  29. Goeres J, Chan PK, Mukhopadhyay D, Zhang H, Raught B, Matunis MJ (2011) The SUMO-specific isopeptidase SENP2 associates dynamically with nuclear pore complexes through interactions with karyopherins and the Nup107-160 nucleoporin subcomplex. Mol Biol Cell 22:4868–4882PubMedPubMedCentralCrossRefGoogle Scholar
  30. Gomez-Cavazos JS, Hetzer MW (2015) The nucleoporin gp210/Nup210 controls muscle differentiation by regulating nuclear envelope/ER homeostasis. J Cell Biol 208:671–681PubMedPubMedCentralCrossRefGoogle Scholar
  31. Gough SM, Slape CI, Aplan PD (2011) NUP98 gene fusions and hematopoietic malignancies: common themes and new biologic insights. Blood 118:6247–6257PubMedPubMedCentralCrossRefGoogle Scholar
  32. Griffis ER, Altan N, Lippincott-Schwartz J, Powers MA (2002) Nup98 is a mobile nucleoporin with transcription-dependent dynamics. Mol Biol Cell 13:1282–1297PubMedPubMedCentralCrossRefGoogle Scholar
  33. Griffis ER, Craige B, Dimaano C, Ullman KS, Powers MA (2004) Distinct functional domains within nucleoporins Nup153 and Nup98 mediate transcription-dependent mobility. Mol Biol Cell 15:1991–2002PubMedPubMedCentralCrossRefGoogle Scholar
  34. Gu Y, Zebell SG, Liang Z, Wang S, Kang BH, Dong X (2016) Nuclear pore permeabilization is a convergent signaling event in effector-triggered immunity. Cell 166:1526–1538.e11PubMedPubMedCentralCrossRefGoogle Scholar
  35. Hang J, Dasso M (2002) Association of the human SUMO-1 protease SENP2 with the nuclear pore. J Biol Chem 277:19961–19966PubMedCrossRefGoogle Scholar
  36. Hattersley N, Cheerambathur D, Moyle M, Stefanutti M, Richardson A, Lee KY, Dumont J, Oegema K, Desai A (2016) A nucleoporin docks protein phosphatase 1 to direct meiotic chromosome segregation and nuclear assembly. Dev Cell 38:463–477PubMedPubMedCentralCrossRefGoogle Scholar
  37. Horigome C, Oma Y, Konishi T, Schmid R, Marcomini I, Hauer MH, Dion V, Harata M, Gasser SM (2014) SWR1 and INO80 chromatin remodelers contribute to DNA double-strand break perinuclear anchorage site choice. Mol Cell 55:626–639PubMedCrossRefGoogle Scholar
  38. Horigome C, Bustard DE, Marcomini I, Delgoshaie N, Tsai-Pflugfelder M, Cobb JA, Gasser SM (2016) PolySUMOylation by Siz2 and Mms21 triggers relocation of DNA breaks to nuclear pores through the Slx5/Slx8 STUbL. Genes Dev 30:931–945PubMedPubMedCentralCrossRefGoogle Scholar
  39. Hu DJ, Baffet AD, Nayak T, Akhmanova A, Doye V, Vallee RB (2013) Dynein recruitment to nuclear pores activates apical nuclear migration and mitotic entry in brain progenitor cells. Cell 154:1300–1313PubMedCrossRefPubMedCentralGoogle Scholar
  40. Ibarra A, Hetzer MW (2015) Nuclear pore proteins and the control of genome functions. Genes Dev 29:337–349PubMedPubMedCentralCrossRefGoogle Scholar
  41. Ibarra A, Benner C, Tyagi S, Cool J, Hetzer MW (2016) Nucleoporin-mediated regulation of cell identity genes. Genes Dev 30:2253–2258PubMedPubMedCentralCrossRefGoogle Scholar
  42. Jacinto FV, Benner C, Hetzer MW (2015) The nucleoporin Nup153 regulates embryonic stem cell pluripotency through gene silencing. Genes Dev 29:1224–1238PubMedPubMedCentralCrossRefGoogle Scholar
  43. Jao LE, Akef A, Wente SR (2017) A role for Gle1, a regulator of DEAD-box RNA helicases, at centrosomes and basal bodies. Mol Biol Cell 28:120–127PubMedPubMedCentralCrossRefGoogle Scholar
  44. Jeganathan KB, Malureanu L, Van Deursen JM (2005) The Rae1-Nup98 complex prevents aneuploidy by inhibiting securin degradation. Nature 438:1036–1039PubMedCrossRefGoogle Scholar
  45. Joseph J, Liu ST, Jablonski SA, Yen TJ, Dasso M (2004) The RanGAP1-RanBP2 complex is essential for microtubule-kinetochore interactions in vivo. Curr Biol 14:611–617PubMedCrossRefGoogle Scholar
  46. Kalocsay M, Hiller NJ, Jentsch S (2009) Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break. Mol Cell 33:335–343PubMedCrossRefGoogle Scholar
  47. Kalverda B, Pickersgill H, Shloma VV, Fornerod M (2010) Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm. Cell 140:360–371PubMedCrossRefGoogle Scholar
  48. Kee HL, Dishinger JF, Blasius TL, Liu CJ, Margolis B, Verhey KJ (2012) A size-exclusion permeability barrier and nucleoporins characterize a ciliary pore complex that regulates transport into cilia. Nat Cell Biol 14:431–437PubMedPubMedCentralCrossRefGoogle Scholar
  49. Kehat I, Accornero F, Aronow BJ, Molkentin JD (2011) Modulation of chromatin position and gene expression by HDAC4 interaction with nucleoporins. J Cell Biol 193:21–29PubMedPubMedCentralCrossRefGoogle Scholar
  50. Khadaroo B, Teixeira MT, Luciano P, Eckert-Boulet N, Germann SM, Simon MN, Gallina I, Abdallah P, Gilson E, Geli V, Lisby M (2009) The DNA damage response at eroded telomeres and tethering to the nuclear pore complex. Nat Cell Biol 11:980–987PubMedCrossRefGoogle Scholar
  51. Knockenhauer KE, Schwartz TU (2016) The nuclear pore complex as a flexible and dynamic gate. Cell 164:1162–1171PubMedPubMedCentralCrossRefGoogle Scholar
  52. Kobayashi A, Hashizume C, Dowaki T, Wong RW (2015) Therapeutic potential of mitotic interaction between the nucleoporin Tpr and aurora kinase A. Cell Cycle 14:1447–1458PubMedPubMedCentralCrossRefGoogle Scholar
  53. Labade AS, Karmodiya K, Sengupta K (2016) HOXA repression is mediated by nucleoporin Nup93 assisted by its interactors Nup188 and Nup205. Epigenetics Chromatin 9:54PubMedPubMedCentralCrossRefGoogle Scholar
  54. Lee SH, Sterling H, Burlingame A, Mccormick F (2008) Tpr directly binds to Mad1 and Mad2 and is important for the Mad1-Mad2-mediated mitotic spindle checkpoint. Genes Dev 22:2926–2931PubMedPubMedCentralCrossRefGoogle Scholar
  55. Lemaitre C, Fischer B, Kalousi A, Hoffbeck AS, Guirouilh-Barbat J, Shahar OD, Genet D, Goldberg M, Betrand P, Lopez B, Brino L, Soutoglou E (2012) The nucleoporin 153, a novel factor in double-strand break repair and DNA damage response. Oncogene 31:4803–4809PubMedCrossRefGoogle Scholar
  56. Liang Y, Franks TM, Marchetto MC, Gage FH, Hetzer MW (2013) Dynamic association of NUP98 with the human genome. PLoS Genet 9:e1003308PubMedPubMedCentralCrossRefGoogle Scholar
  57. Light WH, Freaney J, Sood V, Thompson A, D’Urso A, Horvath CM, Brickner JH (2013) A conserved role for human Nup98 in altering chromatin structure and promoting epigenetic transcriptional memory. PLoS Biol 11:e1001524PubMedPubMedCentralCrossRefGoogle Scholar
  58. Liu J, Prunuske AJ, Fager AM, Ullman KS (2003) The COPI complex functions in nuclear envelope breakdown and is recruited by the nucleoporin Nup153. Dev Cell 5:487–498PubMedCrossRefGoogle Scholar
  59. Loiodice I, Alves A, Rabut G, Van Overbeek M, Ellenberg J, Sibarita JB, Doye V (2004) The entire Nup107-160 complex, including three new members, is targeted as one entity to kinetochores in mitosis. Mol Biol Cell 15:3333–3344PubMedPubMedCentralCrossRefGoogle Scholar
  60. Lupu F, Alves A, Anderson K, Doye V, Lacy E (2008) Nuclear pore composition regulates neural stem/progenitor cell differentiation in the mouse embryo. Dev Cell 14:831–842PubMedPubMedCentralCrossRefGoogle Scholar
  61. Lussi YC, Shumaker DK, Shimi T, Fahrenkrog B (2010) The nucleoporin Nup153 affects spindle checkpoint activity due to an association with Mad1. Nucleus 1:71–84PubMedPubMedCentralCrossRefGoogle Scholar
  62. Mackay DR, Ullman KS (2011) Coordinating postmitotic nuclear pore complex assembly with abscission timing. Nucleus 2:283–288PubMedPubMedCentralCrossRefGoogle Scholar
  63. Mackay DR, Elgort SW, Ullman KS (2009) The nucleoporin Nup153 has separable roles in both early mitotic progression and the resolution of mitosis. Mol Biol Cell 20:1652–1660PubMedPubMedCentralCrossRefGoogle Scholar
  64. Mackay DR, Makise M, Ullman KS (2010) Defects in nuclear pore assembly lead to activation of an Aurora B-mediated abscission checkpoint. J Cell Biol 191:923–931PubMedPubMedCentralCrossRefGoogle Scholar
  65. Maiato H, Gomes AM, Sousa F, Barisic M (2017) Mechanisms of chromosome congression during mitosis. Biology (Basel) 6:13Google Scholar
  66. Malicki JJ, Johnson CA (2017) The cilium: cellular antenna and central processing unit. Trends Cell Biol 27:126–140PubMedPubMedCentralCrossRefGoogle Scholar
  67. Mishra RK, Chakraborty P, Arnaoutov A, Fontoura BM, Dasso M (2010) The Nup107-160 complex and gamma-TuRC regulate microtubule polymerization at kinetochores. Nat Cell Biol 12:164–169PubMedPubMedCentralCrossRefGoogle Scholar
  68. Moorhead GB, Trinkle-Mulcahy L, Nimick M, De Wever V, Campbell DG, Gourlay R, Lam YW, Lamond AI (2008) Displacement affinity chromatography of protein phosphatase one (PP1) complexes. BMC Biochem 9:28PubMedPubMedCentralCrossRefGoogle Scholar
  69. Mossaid I, Fahrenkrog B (2015) Complex commingling: nucleoporins and the spindle assembly checkpoint. Cells 4:706–725PubMedPubMedCentralCrossRefGoogle Scholar
  70. Moudry P, Lukas C, Macurek L, Neumann B, Heriche JK, Pepperkok R, Ellenberg J, Hodny Z, Lukas J, Bartek J (2012) Nucleoporin NUP153 guards genome integrity by promoting nuclear import of 53BP1. Cell Death Differ 19:798–807PubMedCrossRefGoogle Scholar
  71. Nagai S, Dubrana K, Tsai-Pflugfelder M, Davidson MB, Roberts TM, Brown GW, Varela E, Hediger F, Gasser SM, Krogan NJ (2008) Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322:597–602PubMedPubMedCentralCrossRefGoogle Scholar
  72. Nagai S, Heun P, Gasser SM (2010) Roles for nuclear organization in the maintenance of genome stability. Epigenomics 2:289–305PubMedCrossRefGoogle Scholar
  73. Nahse V, Christ L, Stenmark H, Campsteijn C (2017) The abscission checkpoint: making it to the final cut. Trends Cell Biol 27:1–11PubMedCrossRefGoogle Scholar
  74. Nakano H, Funasaka T, Hashizume C, Wong RW (2010) Nucleoporin translocated promoter region (Tpr) associates with dynein complex, preventing chromosome lagging formation during mitosis. J Biol Chem 285:10841–10849PubMedPubMedCentralCrossRefGoogle Scholar
  75. Naylor RM, Jeganathan KB, Cao X, Van Deursen JM (2016) Nuclear pore protein NUP88 activates anaphase-promoting complex to promote aneuploidy. J Clin Invest 126:543–559PubMedPubMedCentralCrossRefGoogle Scholar
  76. Orjalo AV, A A, Shen Z, Boyarchuk Y, Zeitlin SG, Fontoura B, Briggs S, Dasso M, Forbes DJ (2006) The Nup107-160 nucleoporin complex is required for correct bipolar spindle assembly. Mol Biol Cell 17:3806–3818PubMedPubMedCentralCrossRefGoogle Scholar
  77. Palancade B, Liu X, Garcia-Rubio M, Aguilera A, Zhao X, Doye V (2007) Nucleoporins prevent DNA damage accumulation by modulating Ulp1-dependent sumoylation processes. Mol Biol Cell 18:2912–2923PubMedPubMedCentralCrossRefGoogle Scholar
  78. Pascual-Garcia P, Jeong J, Capelson M (2014) Nucleoporin Nup98 associates with Trx/MLL and NSL histone-modifying complexes and regulates Hox gene expression. Cell Rep 9:433–442PubMedCrossRefGoogle Scholar
  79. Pascual-Garcia P, Debo B, Aleman JR, Talamas JA, Lan Y, Nguyen NH, Won KJ, Capelson M (2017) Metazoan nuclear pores provide a scaffold for poised genes and mediate induced enhancer-promoter contacts. Mol Cell 66:63–76.e6PubMedCrossRefGoogle Scholar
  80. Paulsen RD, Soni DV, Wollman R, Hahn AT, Yee MC, Guan A, Hesley JA, Miller SC, Cromwell EF, Solow-Cordero DE, Meyer T, Cimprich KA (2009) A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability. Mol Cell 35:228–239PubMedPubMedCentralCrossRefGoogle Scholar
  81. Platani M, Santarella-mellwig R, Posch M, Walczak R, Swedlow JR, Mattaj IW (2009) The Nup107-160 nucleoporin complex promotes mitotic events via control of the localization state of the chromosome passenger complex. Mol Biol Cell 20:5260–5275PubMedPubMedCentralCrossRefGoogle Scholar
  82. Prevost M, Chamousset D, Nasa I, Freele E, Morrice N, Moorhead G, Trinkle-Mulcahy L (2013) Quantitative fragmentome mapping reveals novel, domain-specific partners for the modular protein RepoMan (recruits PP1 onto mitotic chromatin at anaphase). Mol Cell Proteomics 12:1468–1486PubMedPubMedCentralCrossRefGoogle Scholar
  83. Prunuske AJ, Liu J, elgort S, Joseph J, Dasso M, Ullman KS (2006) Nuclear envelope breakdown is coordinated by both Nup358/RanBP2 and Nup153, two nucleoporins with zinc finger modules. Mol Biol Cell 17:760–769PubMedPubMedCentralCrossRefGoogle Scholar
  84. Ptak C, Wozniak RW (2016) Nucleoporins and chromatin metabolism. Curr Opin Cell Biol 40:153–160PubMedCrossRefGoogle Scholar
  85. Rabut G, Doye V, Ellenberg J (2004) Mapping the dynamic organization of the nuclear pore complex inside single living cells. Nat Cell Biol 6:1114–1121PubMedCrossRefPubMedCentralGoogle Scholar
  86. Raices M, D’Angelo MA (2012) Nuclear pore complex composition: a new regulator of tissue-specific and developmental functions. Nat Rev Mol Cell Biol 13:687–699PubMedCrossRefGoogle Scholar
  87. Raices M, D’Angelo MA (2017) Nuclear pore complexes and regulation of gene expression. Curr Opin Cell Biol 46:26–32PubMedPubMedCentralCrossRefGoogle Scholar
  88. Rasala BA, Orjalo AV, Shen Z, Briggs S, Forbes DJ (2006) ELYS is a dual nucleoporin/kinetochore protein required for nuclear pore assembly and proper cell division. Proc Natl Acad Sci U S A 103:17801–17806PubMedPubMedCentralCrossRefGoogle Scholar
  89. Ritterhoff T, Das H, Hofhaus G, Schroder RR, Flotho A, Melchior F (2016) The RanBP2/RanGAP1*SUMO1/Ubc9 SUMO E3 ligase is a disassembly machine for Crm1-dependent nuclear export complexes. Nat Commun 7:11482PubMedPubMedCentralCrossRefGoogle Scholar
  90. Rout MP, Aitchison JD, Suprapto A, Hjertaas K, Zhao Y, Chait BT (2000) The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol 148:635–651PubMedPubMedCentralCrossRefGoogle Scholar
  91. Sahoo MR, Gaikwad S, Khuperkar D, Ashok M, Helen M, Yadav SK, Singh A, Magre I, Deshmukh P, Dhanvijay S, Sahoo PK, Ramtirtha Y, Madhusudhan MS, Gayathri P, Seshadri V, Joseph J (2017) Nup358 binds to AGO proteins through its SUMO-interacting motifs and promotes the association of target mRNA with miRISC. EMBO Rep 18:241–263PubMedCrossRefGoogle Scholar
  92. Sakin V, Richter SM, Hsiao HH, Urlaub H, Melchior F (2015) Sumoylation of the GTPase Ran by the RanBP2 SUMO E3 ligase complex. J Biol Chem 290:23589–23602PubMedPubMedCentralCrossRefGoogle Scholar
  93. Salina D, Bodoor K, Eckley DM, Schroer TA, Rattner JB, Burke B (2002) Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell 108:97–107PubMedCrossRefGoogle Scholar
  94. Salina D, Enarson P, Rattner JB, Burke B (2003) Nup358 integrates nuclear envelope breakdown with kinetochore assembly. J Cell Biol 162:991–1001PubMedPubMedCentralCrossRefGoogle Scholar
  95. Salsi V, Ferrari S, Gorello P, Fantini S, Chiavolelli F, Mecucci C, Zappavigna V (2014) NUP98 fusion oncoproteins promote aneuploidy by attenuating the mitotic spindle checkpoint. Cancer Res 74:1079–1090PubMedCrossRefGoogle Scholar
  96. Salsi V, Fantini S, Zappavigna V (2016) NUP98 fusion oncoproteins interact with the APC/C(Cdc20) as a pseudosubstrate and prevent mitotic checkpoint complex binding. Cell Cycle 15:2275–2287PubMedPubMedCentralCrossRefGoogle Scholar
  97. Sarmah B, Winfrey VP, Olson GE, Appel B, Wente SR (2007) A role for the inositol kinase Ipk1 in ciliary beating and length maintenance. Proc Natl Acad Sci U S A 104:19843–19848PubMedPubMedCentralCrossRefGoogle Scholar
  98. Schweizer N, Ferras C, Kern DM, Logarinho E, Cheeseman IM, Maiato H (2013) Spindle assembly checkpoint robustness requires Tpr-mediated regulation of Mad1/Mad2 proteostasis. J Cell Biol 203:883–893PubMedPubMedCentralCrossRefGoogle Scholar
  99. Singer S, Zhao R, Barsotti AM, Ouwehand A, Fazollahi M, Coutavas E, Breuhahn K, Neumann O, Longerich T, Pusterla T, Powers MA, Giles KM, Leedman PJ, Hess J, Grunwald D, Bussemaker HJ, Singer RH, Schirmacher P, Prives C (2012) Nuclear pore component Nup98 is a potential tumor suppressor and regulates posttranscriptional expression of select p53 target genes. Mol Cell 48:799–810PubMedPubMedCentralCrossRefGoogle Scholar
  100. Sood V, Brickner JH (2014) Nuclear pore interactions with the genome. Curr Opin Genet Dev 25:43–49PubMedCrossRefGoogle Scholar
  101. Soutoglou E, Misteli T (2007) Mobility and immobility of chromatin in transcription and genome stability. Curr Opin Genet Dev 17:435–442PubMedPubMedCentralCrossRefGoogle Scholar
  102. Splinter D, Tanenbaum ME, Lindqvist A, Jaarsma D, Flotho A, Yu KL, Grigoriev I, Engelsma D, Haasdijk ED, Keijzer N, Demmers J, Fornerod M, Melchior F, Hoogenraad CC, Medema RH, Akhmanova A (2010) Bicaudal D2, dynein, and kinesin-1 associate with nuclear pore complexes and regulate centrosome and nuclear positioning during mitotic entry. PLoS Biol 8:e1000350PubMedPubMedCentralCrossRefGoogle Scholar
  103. Splinter D, Razafsky DS, Schlager MA, Serra-Marques A, Grigoriev I, Demmers J, Keijzer N, Jiang K, Poser I, Hyman AA, Hoogenraad CC, King SJ, Akhmanova A (2012) BICD2, dynactin, and LIS1 cooperate in regulating dynein recruitment to cellular structures. Mol Biol Cell 23:4226–4241PubMedPubMedCentralCrossRefGoogle Scholar
  104. Stavru F, Nautrup-Pedersen G, Cordes VC, Gorlich D (2006) Nuclear pore complex assembly and maintenance in POM121- and gp210-deficient cells. J Cell Biol 173:477–483PubMedPubMedCentralCrossRefGoogle Scholar
  105. Steigemann P, Wurzenberger C, Schmitz MH, Held M, Guizetti J, Maar S, Gerlich DW (2009) Aurora B-mediated abscission checkpoint protects against tetraploidization. Cell 136:473–484PubMedCrossRefGoogle Scholar
  106. Su XA, Dion V, Gasser SM, Freudenreich CH (2015) Regulation of recombination at yeast nuclear pores controls repair and triplet repeat stability. Genes Dev 29:1006–1017PubMedPubMedCentralCrossRefGoogle Scholar
  107. Takao D, Dishinger JF, Kee HL, Pinskey JM, Allen BL, Verhey KJ (2014) An assay for clogging the ciliary pore complex distinguishes mechanisms of cytosolic and membrane protein entry. Curr Biol 24:2288–2294PubMedPubMedCentralCrossRefGoogle Scholar
  108. Toyama BH, Savas JN, Park SK, Harris MS, Ingolia NT, Yates JR 3rd, Hetzer MW (2013) Identification of long-lived proteins reveals exceptional stability of essential cellular structures. Cell 154:971–982PubMedPubMedCentralCrossRefGoogle Scholar
  109. Ungricht R, Kutay U (2017) Mechanisms and functions of nuclear envelope remodelling. Nat Rev Mol Cell Biol 18:229–245PubMedCrossRefGoogle Scholar
  110. Vagnarelli P, Ribeiro S, Sennels L, Sanchez-Pulido L, De Lima Alves F, Verheyen T, Kelly DA, Ponting CP, Rappsilber J, Earnshaw WC (2011) Repo-Man coordinates chromosomal reorganization with nuclear envelope reassembly during mitotic exit. Dev Cell 21:328–342PubMedCrossRefGoogle Scholar
  111. Vaquerizas JM, Suyama R, Kind J, Miura K, Luscombe NM, Akhtar A (2010) Nuclear pore proteins nup153 and megator define transcriptionally active regions in the Drosophila genome. PLoS Genet 6:e1000846PubMedPubMedCentralCrossRefGoogle Scholar
  112. Vecchione L, Gambino V, Raaijmakers J, Schlicker A, Fumagalli A, Russo M, Villanueva A, Beerling E, Bartolini A, Mollevi DG, El-Murr N, Chiron M, Calvet L, Nicolazzi C, Combeau C, Henry C, Simon IM, Tian S, In ’t Veld S, D’Ario G, Mainardi S, Beijersbergen RL, Lieftink C, Linn S, Rumpf-Kienzl C, Delorenzi M, Wessels L, Salazar R, Di Nicolantonio F, Bardelli A, Van Rheenen J, Medema RH, Tejpar S, Bernards R (2016) A vulnerability of a subset of colon cancers with potential clinical utility. Cell 165:317–330PubMedCrossRefGoogle Scholar
  113. Wang GG, Cai L, Pasillas MP, Kamps MP (2007) NUP98-NSD1 links H3K36 methylation to Hox-A gene activation and leukaemogenesis. Nat Cell Biol 9:804–812PubMedCrossRefGoogle Scholar
  114. Wang GG, Song J, Wang Z, Dormann HL, Casadio F, Li H, Luo JL, Patel DJ, Allis CD (2009) Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. Nature 459:847–851PubMedPubMedCentralCrossRefGoogle Scholar
  115. Werner A, Flotho A, Melchior F (2012) The RanBP2/RanGAP1*SUMO1/Ubc9 complex is a multisubunit SUMO E3 ligase. Mol Cell 46:287–298PubMedCrossRefGoogle Scholar
  116. Zhang H, Saitoh H, Matunis MJ (2002) Enzymes of the SUMO modification pathway localize to filaments of the nuclear pore complex. Mol Cell Biol 22:6498–6508PubMedPubMedCentralCrossRefGoogle Scholar
  117. Zuccolo M, Alves A, Galy V, Bolhy S, Formstecher E, Racine V, Sibarita JB, Fukagawa T, Shiekhattar R, Yen T, Doye V (2007) The human Nup107-160 nuclear pore subcomplex contributes to proper kinetochore functions. EMBO J 26:1853–1864PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Oncological SciencesHuntsman Cancer Institute, University of UtahSalt Lake CityUSA

Personalised recommendations