Poring over pores: Nuclear pore complex insertion into the nuclear envelope

Trends in Biochemical Sciences

Volumn 38, Issue 6, 2013, Pages 292-301

  Rothballer, Andrea ^a   Kutay, Ulrike ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Biogenesis; Membrane fusion; Nuclear envelope; Nuclear pore complex; Nucleoporin

Indexed keywords

MEMBRANE PROTEIN;

BIOGENESIS; BIOPHYSICS; CARBOXY TERMINAL SEQUENCE; CELL COMPARTMENTALIZATION; CELL GROWTH; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL VACUOLE; CYTOCHEMISTRY; CYTOPLASM; HUMAN; INTERPHASE; MEMBRANE BINDING; MEMBRANE BIOLOGY; MEMBRANE STABILIZATION; MEMBRANE STRUCTURE; MOLECULAR MODEL; NONHUMAN; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROTEIN ASSEMBLY; REVIEW;

NUCLEAR ENVELOPE; NUCLEAR PORE;

EID: 84878118654     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2013.04.001     Document Type: Review

References (103)

1. Hetzer M.W., Wente S.R. Border control at the nucleus: biogenesis and organization of the nuclear membrane and pore complexes. Dev. Cell 2009, 17:606-616.
2. Grossman E., et al. Functional architecture of the nuclear pore complex. Annu. Rev. Biophys. 2012, 41:557-584.
3. Hoelz A., et al. The structure of the nuclear pore complex. Annu. Rev. Biochem. 2011, 80:613-643.
4. Terry L.J., Wente S.R. Flexible gates: dynamic topologies and functions for FG nucleoporins in nucleocytoplasmic transport. Eukaryot. Cell 2009, 8:1814-1827.
5. Wente S.R., Rout M.P. The nuclear pore complex and nuclear transport. Cold Spring Harb. Perspect. Biol. 2010, 2:a000562.
6. Kahms M., et al. Lighting up the nuclear pore complex. Eur. J. Cell Biol. 2011, 90:751-758.
7. Guttinger S., et al. Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat. Rev. Mol. Cell Biol. 2009, 10:178-191.
8. Wandke C., Kutay U. Enclosing chromatin: reassembly of the nucleus after open mitosis. Cell 2013, 152:1222-1225.
9. Schooley A., et al. Building a nuclear envelope at the end of mitosis: coordinating membrane reorganization, nuclear pore complex assembly, and chromatin de-condensation. Chromosoma 2012, 121:539-554.
10. Antonin W., et al. Nuclear pore complex assembly through the cell cycle: regulation and membrane organization. FEBS Lett. 2008, 582:2004-2016.
11. Doucet C.M., Hetzer M.W. Nuclear pore biogenesis into an intact nuclear envelope. Chromosoma 2010, 119:469-477.
12. Rabut G., et al. Dynamics of nuclear pore complex organization through the cell cycle. Curr. Opin. Cell Biol. 2004, 16:314-321.
13. Martens S., McMahon H.T. Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol. 2008, 9:543-556.
14. Kozlov M.M., et al. Protein-driven membrane stresses in fusion and fission. Trends Biochem. Sci. 2010, 35:699-706.
15. Campelo F., Malhotra V. Membrane fission: the biogenesis of transport carriers. Annu. Rev. Biochem. 2012, 81:407-427.
16. Savas J.N., et al. Extremely long-lived nuclear pore proteins in the rat brain. Science 2012, 335:942.
17. D'Angelo M.A., et al. Age-dependent deterioration of nuclear pore complexes causes a loss of nuclear integrity in postmitotic cells. Cell 2009, 136:284-295.
18. Harrison S.C. Viral membrane fusion. Nat. Struct. Mol. Biol. 2008, 15:690-698.
19. Sudhof T.C., Rothman J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 2009, 323:474-477.
20. Neumann N., et al. Comparative genomic evidence for a complete nuclear pore complex in the last eukaryotic common ancestor. PLoS ONE 2010, 5:e13241.
21. Chadrin A., et al. Pom33, a novel transmembrane nucleoporin required for proper nuclear pore complex distribution. J. Cell Biol. 2010, 189:795-811.
22. Stavru F., et al. NDC1: a crucial membrane-integral nucleoporin of metazoan nuclear pore complexes. J. Cell Biol. 2006, 173:509-519.
23. Mansfeld J., et al. The conserved transmembrane nucleoporin NDC1 is required for nuclear pore complex assembly in vertebrate cells. Mol. Cell 2006, 22:93-103.
24. Miao M., et al. The integral membrane protein Pom34p functionally links nucleoporin subcomplexes. Genetics 2006, 172:1441-1457.
25. Lau C.K., et al. A novel allele of Saccharomyces cerevisiae NDC1 reveals a potential role for the spindle pole body component Ndc1p in nuclear pore assembly. Eukaryot. Cell 2004, 3:447-458.
26. Gerace L., et al. Identification of a major polypeptide of the nuclear pore complex. J. Cell Biol. 1982, 95:826-837.
27. Wozniak R.W., et al. POM152 is an integral protein of the pore membrane domain of the yeast nuclear envelope. J. Cell Biol. 1994, 125:31-42.
28. Hallberg E., et al. An integral membrane protein of the pore membrane domain of the nuclear envelope contains a nucleoporin-like region. J. Cell Biol. 1993, 122:513-521.
29. Madrid A.S., et al. The role of the integral membrane nucleoporins Ndc1p and Pom152p in nuclear pore complex assembly and function. J. Cell Biol. 2006, 173:361-371.
30. Winey M., et al. NDC1: a nuclear periphery component required for yeast spindle pole body duplication. J. Cell Biol. 1993, 122:743-751.
31. West R.R., et al. cut11(+): A gene required for cell cycle-dependent spindle pole body anchoring in the nuclear envelope and bipolar spindle formation in Schizosaccharomyces pombe. Mol. Biol. Cell 1998, 9:2839-2855.
32. Jaspersen S.L., Winey M. The budding yeast spindle pole body: structure, duplication, and function. Annu. Rev. Cell Dev. Biol. 2004, 20:1-28.
33. Jaspersen S.L., Ghosh S. Nuclear envelope insertion of spindle pole bodies and nuclear pore complexes. Nucleus 2012, 3:226-236.
34. Onischenko E., et al. Role of the Ndc1 interaction network in yeast nuclear pore complex assembly and maintenance. J. Cell Biol. 2009, 185:475-491.
35. Mans B.J., et al. Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex. Cell Cycle 2004, 3:1612-1637.
36. Olsson M., et al. cDNA cloning and embryonic expression of mouse nuclear pore membrane glycoprotein 210 mRNA. Kidney Int. 1999, 56:827-838.
37. Wozniak R.W., et al. Primary structure analysis of an integral membrane glycoprotein of the nuclear pore. J. Cell Biol. 1989, 108:2083-2092.
38. Tcheperegine S.E., et al. Topology and functional domains of the yeast pore membrane protein Pom152p. J. Biol. Chem. 1999, 274:5252-5258.
39. Funakoshi T., et al. Localization of Pom121 to the inner nuclear membrane is required for an early step of interphase nuclear pore complex assembly. Mol. Biol. Cell 2011, 22:1058-1069.
40. Doucet C.M., et al. Cell cycle-dependent differences in nuclear pore complex assembly in metazoa. Cell 2010, 141:1030-1041.
41. Antonin W., et al. The integral membrane nucleoporin pom121 functionally links nuclear pore complex assembly and nuclear envelope formation. Mol. Cell 2005, 17:83-92.
42. Yavuz S., et al. NLS-mediated NPC functions of the nucleoporin Pom121. FEBS Lett. 2010, 584:3292-3298.
43. Soderqvist H., Hallberg E. The large C-terminal region of the integral pore membrane protein, POM121, is facing the nuclear pore complex. Eur. J. Cell Biol. 1994, 64:186-191.
44. Talamas J.A., Hetzer M.W. POM121 and Sun1 play a role in early steps of interphase NPC assembly. J. Cell Biol. 2011, 194:27-37.
45. Liu Q., et al. Functional association of Sun1 with nuclear pore complexes. J. Cell Biol. 2007, 178:785-798.
46. 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. 2010, 26:421-444.
47. Friederichs J.M., et al. The SUN protein Mps3 is required for spindle pole body insertion into the nuclear membrane and nuclear envelope homeostasis. PLoS Genet. 2011, 7:e1002365.
48. Jaspersen S.L., et al. Mps3p is a novel component of the yeast spindle pole body that interacts with the yeast centrin homologue Cdc31p. J. Cell Biol. 2002, 159:945-956.
49. Witkin K.L., et al. Changes in the nuclear envelope environment affect spindle pole body duplication in Saccharomyces cerevisiae. Genetics 2010, 186:867-883.
50. Yewdell W.T., et al. Lumenal interactions in nuclear pore complex assembly and stability. Mol. Biol. Cell 2011, 22:1375-1388.
51. Brachner A., Foisner R. Evolvement of LEM proteins as chromatin tethers at the nuclear periphery. Biochem. Soc. Trans. 2011, 39:1735-1741.
52. Devos D., et al. Simple fold composition and modular architecture of the nuclear pore complex. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:2172-2177.
53. Devos D., et al. Components of coated vesicles and nuclear pore complexes share a common molecular architecture. PLoS Biol. 2004, 2:e380.
54. Brohawn S.G., et al. Structural evidence for common ancestry of the nuclear pore complex and vesicle coats. Science 2008, 322:1369-1373.
55. Hawryluk-Gara L.A., et al. Vertebrate Nup53 interacts with the nuclear lamina and is required for the assembly of a Nup93-containing complex. Mol. Biol. Cell 2005, 16:2382-2394.
56. Marelli M., et al. Specific binding of the karyopherin Kap121p to a subunit of the nuclear pore complex containing Nup53p, Nup59p, and Nup170p. J. Cell Biol. 1998, 143:1813-1830.
57. Vollmer B., et al. Dimerization and direct membrane interaction of Nup53 contribute to nuclear pore complex assembly. EMBO J. 2012, 31:4072-4084.
58. Mitchell J.M., et al. Pom121 links two essential subcomplexes of the nuclear pore complex core to the membrane. J. Cell Biol. 2010, 191:505-521.
59. Makio T., et al. The nucleoporins Nup170p and Nup157p are essential for nuclear pore complex assembly. J. Cell Biol. 2009, 185:459-473.
60. Flemming D., et al. Two structurally distinct domains of the nucleoporin Nup170 cooperate to tether a subset of nucleoporins to nuclear pores. J. Cell Biol. 2009, 185:387-395.
61. Lusk C.P., et al. Karyopherins in nuclear pore biogenesis: a role for Kap121p in the assembly of Nup53p into nuclear pore complexes. J. Cell Biol. 2002, 159:267-278.
62. Hawryluk-Gara L.A., et al. Nup53 is required for nuclear envelope and nuclear pore complex assembly. Mol. Biol. Cell 2008, 19:1753-1762.
63. Drin G., et al. A general amphipathic alpha-helical motif for sensing membrane curvature. Nat. Struct. Mol. Biol. 2007, 14:138-146.
64. Walther T.C., et al. The conserved Nup107-160 complex is critical for nuclear pore complex assembly. Cell 2003, 113:195-206.
65. Harel A., et al. Removal of a single pore subcomplex results in vertebrate nuclei devoid of nuclear pores. Mol. Cell 2003, 11:853-864.
66. Dultz E., Ellenberg J. Live imaging of single nuclear pores reveals unique assembly kinetics and mechanism in interphase. J. Cell Biol. 2010, 191:15-22.
67. Drin G., Antonny B. Amphipathic helices and membrane curvature. FEBS Lett. 2010, 584:1840-1847.
68. Li O., et al. Mutation or deletion of the Saccharomyces cerevisiae RAT3/NUP133 gene causes temperature-dependent nuclear accumulation of poly(A)+ RNA and constitutive clustering of nuclear pore complexes. Mol. Biol. Cell 1995, 6:401-417.
69. Pemberton L.F., et al. Disruption of the nucleoporin gene NUP133 results in clustering of nuclear pore complexes. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:1187-1191.
70. Doye V., et al. A novel nuclear pore protein Nup133p with distinct roles in poly(A)+ RNA transport and nuclear pore distribution. EMBO J. 1994, 13:6062-6075.
71. Hu J., et al. Weaving the web of ER tubules. Cell 2011, 147:1226-1231.
72. Dawson T.R., et al. ER membrane-bending proteins are necessary for de novo nuclear pore formation. J. Cell Biol. 2009, 184:659-675.
73. 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 2012, 192:441-455.
74. Grandi P., et al. Functional interaction of Nic96p with a core nucleoporin complex consisting of Nsp1p, Nup49p and a novel protein Nup57p. EMBO J. 1995, 14:76-87.
75. Sachdev R., et al. The C-terminal domain of Nup93 is essential for assembly of the structural backbone of nuclear pore complexes. Mol. Biol. Cell 2012, 23:740-749.
76. Grandi P., et al. Nup93, a vertebrate homologue of yeast Nic96p, forms a complex with a novel 205-kDa protein and is required for correct nuclear pore assembly. Mol. Biol. Cell 1997, 8:2017-2038.
77. Zabel U., et al. Nic96p is required for nuclear pore formation and functionally interacts with a novel nucleoporin, Nup188p. J. Cell Biol. 1996, 133:1141-1152.
78. Amlacher S., et al. Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile. Cell 2011, 146:277-289.
79. Hulsmann B.B., et al. The permeability of reconstituted nuclear pores provides direct evidence for the selective phase model. Cell 2012, 150:738-751.
80. Laurell E., et al. Phosphorylation of Nup98 by multiple kinases is crucial for NPC disassembly during mitotic entry. Cell 2011, 144:539-550.
81. Griffis E.R., et al. Nup98 localizes to both nuclear and cytoplasmic sides of the nuclear pore and binds to two distinct nucleoporin subcomplexes. Mol. Biol. Cell 2003, 14:600-610.
82. Fontoura B.M., et al. A conserved biogenesis pathway for nucleoporins: proteolytic processing of a 186-kilodalton precursor generates Nup98 and the novel nucleoporin, Nup96. J. Cell Biol. 1999, 144:1097-1112.
83. Stuwe T., et al. Molecular basis for the anchoring of proto-oncoprotein Nup98 to the cytoplasmic face of the nuclear pore complex. J. Mol. Biol. 2012, 419:330-346.
84. Maul G.G., et al. Formation and distribution of nuclear pore complexes in interphase. J. Cell Biol. 1971, 51:405-418.
85. Maeshima K., et al. Nuclear pore formation but not nuclear growth is governed by cyclin-dependent kinases (Cdks) during interphase. Nat. Struct. Mol. Biol. 2010, 17:1065-1071.
86. D'Angelo M.A., et al. Nuclear pores form de novo from both sides of the nuclear envelope. Science 2006, 312:440-443.
87. Levy D.L., Heald R. Mechanisms of intracellular scaling. Annu. Rev. Cell Dev. Biol. 2012, 28:113-135.
88. Anderson D.J., Hetzer M.W. Nuclear envelope formation by chromatin-mediated reorganization of the endoplasmic reticulum. Nat. Cell Biol. 2007, 9:1160-1166.
89. Prufert K., et al. The lamin CxxM motif promotes nuclear membrane growth. J. Cell Sci. 2004, 117:6105-6116.
90. Marelli M., et al. A link between the synthesis of nucleoporins and the biogenesis of the nuclear envelope. J. Cell Biol. 2001, 153:709-724.
91. Brandt A., et al. Developmental control of nuclear size and shape by Kugelkern and Kurzkern. Curr. Biol. 2006, 16:543-552.
92. Bastos R., et al. Targeting and function in mRNA export of nuclear pore complex protein Nup153. J. Cell Biol. 1996, 134:1141-1156.
93. Theerthagiri G., et al. The nucleoporin Nup188 controls passage of membrane proteins across the nuclear pore complex. J. Cell Biol. 2010, 189:1129-1142.
94. Shaulov L., et al. A dominant-negative form of POM121 binds chromatin and disrupts the two separate modes of nuclear pore assembly. J. Cell Sci. 2011, 124:3822-3834.
95. Ferguson S.M., De Camilli P. Dynamin, a membrane-remodelling GTPase. Nat. Rev. Mol. Cell Biol. 2012, 13:75-88.
96. McMahon H.T., Gallop J.L. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 2005, 438:590-596.
97. Shen H., et al. SnapShot: membrane curvature sensors and generators. Cell 2012, 150:1300-1302.
98. Graham T.R., Kozlov M.M. Interplay of proteins and lipids in generating membrane curvature. Curr. Opin. Cell Biol. 2010, 22:430-436.
99. Lin S., et al. Molecular basis for sculpting the endoplasmic reticulum membrane. Int. J. Biochem. Cell Biol. 2012, 44:1436-1443.
100. Simons K., Vaz W.L. Model systems, lipid rafts, and cell membranes. Annu. Rev. Biophys. Biomol. Struct. 2004, 33:269-295.
101. Scarcelli J.J., et al. The yeast integral membrane protein Apq12 potentially links membrane dynamics to assembly of nuclear pore complexes. J. Cell Biol. 2007, 178:799-812.
102. Hodge C.A., et al. Integral membrane proteins Brr6 and Apq12 link assembly of the nuclear pore complex to lipid homeostasis in the endoplasmic reticulum. J. Cell Sci. 2010, 123:141-151.
103. Tamm T., et al. Brr6 drives the Schizosaccharomyces pombe spindle pole body nuclear envelope insertion/extrusion cycle. J. Cell Biol. 2011, 195:467-484.