Nuclear envelope and genome interactions in cell fate

Frontiers in Genetics

Volumn 5, Issue FEB, 2015, Pages

  Talamas, Jessica A ^a   Capelson, Maya ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSKELETON PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GAMMA INTERFERON; LAMIN A; LAMIN B; LAMIN C; MEMBRANE PROTEIN; NUCLEAR MEMBRANE PROTEIN; NUCLEOPORIN; PROTEOME; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL DIVISION; CELL FATE; CELL NUCLEUS MEMBRANE; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME 5; DROSOPHILA; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INTERACTION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; GENOME; HELA CELL LINE; HETEROCHROMATIN; HUMAN; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; LIPID MEMBRANE; MITOSIS; NONHUMAN; NUCLEAR LAMINA; NUCLEAR PORE COMPLEX; ORGANOGENESIS; PROTEIN EXPRESSION; PROTEOMICS; RNA INTERFERENCE; RNA SEQUENCE; SEQUENCE ANALYSIS; TISSUE SPECIFICITY;

EUKARYOTA;

EID: 84923609539     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2015.00095     Document Type: Article

References (160)

1. Ahmed, K., Dehghani, H., Rugg-Gunn, P., Fussner, E., Rossant, J., and Bazett- Jones, D.P. (2010). Global chromatin architecture reflects pluripotency and lineage commitment in the early mouse embryo. PLoS One 5, e10531. doi: 10.1371/journal.pone.0010531.
2. Akhtar, A., and Gasser, S.M. (2007). The nuclear envelope and transcriptional control. Nat Rev Genet 8, 507-517. doi: 10.1038/nrg2122.
3. Amendola, M., and Van Steensel, B. (2014). Mechanisms and dynamics of nuclear lamina-genome interactions. Curr Opin Cell Biol 28, 61-68. doi: 10.1016/j.ceb.2014.03.003.
4. Apel, E.D., Lewis, R.M., Grady, R.M., and Sanes, J.R. (2000). Syne-1, a dystrophin- and Klarsicht-related protein associated with synaptic nuclei at the neuromuscular junction. J Biol Chem 275, 31986-31995. doi: 10.1074/jbc.M004775200.
5. Arib, G., and Akhtar, A. (2011). Multiple facets of nuclear periphery in gene expression control. Curr Opin Cell Biol 23, 346-353. doi: S0955- 0674(10)00218-8 [pii] 10.1016/j.ceb.2010.12.005.
6. Bartova, E., Galiova, G., Krejci, J., Harnicarova, A., Strasak, L., and Kozubek, S. (2008). Epigenome and chromatin structure in human embryonic stem cells undergoing differentiation. Dev Dyn 237, 3690-3702. doi: 10.1002/dvdy.21773.
7. Basel-Vanagaite, L., Muncher, L., Straussberg, R., Pasmanik-Chor, M., Yahav, M., Rainshtein, L., Walsh, C.A., Magal, N., Taub, E., Drasinover, V., Shalev, H., Attia, R., Rechavi, G., Simon, A.J., and Shohat, M. (2006). Mutated nup62 causes autosomal recessive infantile bilateral striatal necrosis. Ann Neurol 60, 214-222.
8. Bickmore, W.A., and Van Steensel, B. (2013). Genome architecture: domain organization of interphase chromosomes. Cell 152, 1270-1284. doi: S0092-8674(13)00146-3 [pii] 10.1016/j.cell.2013.02.001.
9. Blobel, G. (1985). Gene gating: a hypothesis. Proc Natl Acad Sci U S A 82, 8527-8529.
10. Boskovic, A., Eid, A., Pontabry, J., Ishiuchi, T., Spiegelhalter, C., Raghu Ram, E.V., Meshorer, E., and Torres-Padilla, M.E. (2014). Higher chromatin mobility supports totipotency and precedes pluripotency in vivo. Genes Dev 28, 1042-1047. doi: 10.1101/gad.238881.114.
11. Brickner, D.G., Ahmed, S., Meldi, L., Thompson, A., Light, W., Young, M., Hickman, T.L., Chu, F., Fabre, E., and Brickner, J.H. (2012). Transcription factor binding to a DNA zip code controls interchromosomal clustering at the nuclear periphery. Dev Cell 22, 1234-1246. doi: S1534- 5807(12)00135-9 [pii] 10.1016/j.devcel.2012.03.012.
12. Broers, J.L., Kuijpers, H.J., Ostlund, C., Worman, H.J., Endert, J., and Ramaekers, F.C. (2005). Both lamin A and lamin C mutations cause lamina instability as well as loss of internal nuclear lamin organization. Exp Cell Res 304, 582-592. doi: 10.1016/j.yexcr.2004.11.020.
13. Brown, C.R., Kennedy, C.J., Delmar, V.A., Forbes, D.J., and Silver, P.A. (2008). Global histone acetylation induces functional genomic reorganization at mammalian nuclear pore complexes. Genes Dev 22, 627-639.
14. Bruston, F., Delbarre, E., Ostlund, C., Worman, H.J., Buendia, B., and Duband- Goulet, I. (2010). Loss of a DNA binding site within the tail of prelamin A contributes to altered heterochromatin anchorage by progerin. FEBS Lett 584, 2999-3004. doi: 10.1016/j.febslet.2010.05.032.
15. Cabal, G.G., Genovesio, A., Rodriguez-Navarro, S., Zimmer, C., Gadal, O., Lesne, A., Buc, H., Feuerbach-Fournier, F., Olivo-Marin, J.C., Hurt, E.C., and Nehrbass, U. (2006). SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature 441, 770-773.
16. Capelson, M., and Hetzer, M.W. (2009). The role of nuclear pores in gene regulation, development and disease. EMBO Rep 10, 697-705. doi: embor2009147 [pii] 10.1038/embor.2009.147.
17. Capelson, M., Liang, Y., Schulte, R., Mair, W., Wagner, U., and Hetzer, M.W. (2010). Chromatin-bound nuclear pore components regulate gene expression in higher eukaryotes. Cell 140, 372-383. doi: S0092- 8674(09)01681-X [pii] 10.1016/j.cell.2009.12.054.
18. Casolari, J.M., Brown, C.R., Drubin, D.A., Rando, O.J., and Silver, P.A. (2005). Developmentally induced changes in transcriptional program alter spatial organization across chromosomes. Genes Dev 19, 1188-1198.
19. Casolari, J.M., Brown, C.R., Komili, S., West, J., Hieronymus, H., and Silver, P.A. (2004). Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 117, 427-439.
20. Chahine, M.N., Mioulane, M., Sikkel, M.B., O'gara, P., Dos Remedios, C.G., Pierce, G.N., Lyon, A.R., Foldes, G., and Harding, S.E. (2014). Nuclear pore rearrangements and nuclear trafficking in cardiomyocytes from rat and human failing hearts. Cardiovasc Res. doi: 10.1093/cvr/cvu218.
21. Chen, H., Chen, X., and Zheng, Y. (2013). The nuclear lamina regulates germline stem cell niche organization via modulation of EGFR signaling. Cell Stem Cell 13, 73-86. doi: 10.1016/j.stem.2013.05.003.
22. Chow, K.H., Factor, R.E., and Ullman, K.S. (2012). The nuclear envelope environment and its cancer connections. Nat Rev Cancer 12, 196-209. doi: 10.1038/nrc3219.
23. Collin, L., Schlessinger, K., and Hall, A. (2008). APC nuclear membrane association and microtubule polarity. Biol Cell 100, 243-252. doi: 10.1042/BC20070123.
24. Combs, P.A., and Eisen, M.B. (2013). Sequencing mRNA from cryo-sliced Drosophila embryos to determine genome-wide spatial patterns of gene expression. PLoS One 8, e71820. doi: 10.1371/journal.pone.0071820.
25. Constantinescu, D., Gray, H.L., Sammak, P.J., Schatten, G.P., and Csoka, A.B. (2006). Lamin A/C expression is a marker of mouse and human embryonic stem cell differentiation. Stem Cells 24, 177-185. doi: 10.1634/stemcells.2004-0159.
26. Crisp, M., Liu, Q., Roux, K., Rattner, J.B., Shanahan, C., Burke, B., Stahl, P.D., and Hodzic, D. (2006). Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 172, 41-53. doi: 10.1083/jcb.200509124.
27. D'angelo, M.A., Gomez-Cavazos, J.S., Mei, A., Lackner, D.H., and Hetzer, M.W. (2012). A change in nuclear pore complex composition regulates cell differentiation. Dev Cell 22, 446-458. doi: 10.1016/j.devcel.2011.11.021.
28. D'angelo, M.A., and Hetzer, M.W. (2008a). Lifelong stability of nuclear pore complexes in post-mitotic cells. Cell under revision.
29. D'angelo, M.A., and Hetzer, M.W. (2008b). Structure, dynamics and function of nuclear pore complexes. Trends Cell Biol 18, 456-466.
30. Dauer, W.T., and Worman, H.J. (2009). The nuclear envelope as a signaling node in development and disease. Dev Cell 17, 626-638. doi: S1534- 5807(09)00438-9 [pii] 10.1016/j.devcel.2009.10.016.
31. Davuluri, G., Gong, W., Yusuff, S., Lorent, K., Muthumani, M., Dolan, A.C., and Pack, M. (2008). Mutation of the zebrafish nucleoporin elys sensitizes tissue progenitors to replication stress. PLoS Genet 4, e1000240.
32. De Jong-Curtain, T.A., Parslow, A.C., Trotter, A.J., Hall, N.E., Verkade, H., Tabone, T., Christie, E.L., Crowhurst, M.O., Layton, J.E., Shepherd, I.T., Nixon, S.J., Parton, R.G., Zon, L.I., Stainier, D.Y., Lieschke, G.J., and Heath, J.K. (2008). Abnormal Nuclear Pore Formation Triggers Apoptosis in the Intestinal Epithelium of elys-Deficient Zebra Fish. Gastroenterology.
33. Dittmar, K.A., Goodenbour, J.M., and Pan, T. (2006). Tissue-specific differences in human transfer RNA expression. PLoS Genet 2, e221. doi: 10.1371/journal.pgen.0020221.
34. Dittmer, T.A., and Misteli, T. (2011). The lamin protein family. Genome Biol 12, 222. doi: 10.1186/gb-2011-12-5-222.
35. Dreger, M., Bengtsson, L., Schoneberg, T., Otto, H., and Hucho, F. (2001). Nuclear envelope proteomics: novel integral membrane proteins of the inner nuclear membrane. Proc Natl Acad Sci U S A 98, 11943-11948. doi: 10.1073/pnas.211201898.
36. Duong, N.T., Morris, G.E., Lam Le, T., Zhang, Q., Sewry, C.A., Shanahan, C.M., and Holt, I. (2014). Nesprins: tissue-specific expression of epsilon and other short isoforms. PLoS One 9, e94380. doi: 10.1371/journal.pone.0094380.
37. Eberhart, A., Feodorova, Y., Song, C., Wanner, G., Kiseleva, E., Furukawa, T., Kimura, H., Schotta, G., Leonhardt, H., Joffe, B., and Solovei, I. (2013). Epigenetics of eu- and heterochromatin in inverted and conventional nuclei from mouse retina. Chromosome Res 21, 535-554. doi: 10.1007/s10577-013-9375-7.
38. Eckersley-Maslin, M.A., Bergmann, J.H., Lazar, Z., and Spector, D.L. (2013). Lamin A/C is expressed in pluripotent mouse embryonic stem cells. Nucleus 4, 53-60. doi: 10.4161/nucl.23384.
39. Efroni, S., Duttagupta, R., Cheng, J., Dehghani, H., Hoeppner, D.J., Dash, C., Bazett-Jones, D.P., Le Grice, S., Mckay, R.D., Buetow, K.H., Gingeras, T.R., Misteli, T., and Meshorer, E. (2008). Global transcription in pluripotent embryonic stem cells. Cell Stem Cell 2, 437-447. doi: 10.1016/j.stem.2008.03.021.
40. Finlan, L.E., Sproul, D., Thomson, I., Boyle, S., Kerr, E., Perry, P., Ylstra, B., Chubb, J.R., and Bickmore, W.A. (2008). Recruitment to the nuclear periphery can alter expression of genes in human cells. PLoS Genet 4, e1000039. doi: 10.1371/journal.pgen.1000039.
41. Galy, V., Mattaj, I.W., and Askjaer, P. (2003). Caenorhabditis elegans nucleoporins Nup93 and Nup205 determine the limit of nuclear pore complex size exclusion in vivo. Mol Biol Cell 14, 5104-5115.
42. Gigliotti, S., Callaini, G., Andone, S., Riparbelli, M.G., Pernas-Alonso, R., Hoffmann, G., Graziani, F., and Malva, C. (1998). Nup154, a new Drosophila gene essential for male and female gametogenesis is related to the nup155 vertebrate nucleoporin gene. J Cell Biol 142, 1195-1207.
43. Goldberg, M.W., Huttenlauch, I., Hutchison, C.J., and Stick, R. (2008). Filaments made from A- and B-type lamins differ in structure and organization. J Cell Sci 121, 215-225. doi: 10.1242/jcs.022020.
44. Gomez-Cavazos, J.S., and Hetzer, M.W. (2012). Outfits for different occasions: tissue-specific roles of Nuclear Envelope proteins. Curr Opin Cell Biol 24, 775-783. doi: 10.1016/j.ceb.2012.08.008.
45. Guelen, L., Pagie, L., Brasset, E., Meuleman, W., Faza, M.B., Talhout, W., Eussen, B.H., De Klein, A., Wessels, L., De Laat, W., and Van Steensel, B. (2008). Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453, 948-951. doi: 10.1038/nature06947.
46. Haque, F., Mazzeo, D., Patel, J.T., Smallwood, D.T., Ellis, J.A., Shanahan, C.M., and Shackleton, S. (2010). Mammalian SUN protein interaction networks at the inner nuclear membrane and their role in laminopathy disease processes. J Biol Chem 285, 3487-3498. doi: 10.1074/jbc.M109.071910.
47. Hirano, Y., Hizume, K., Kimura, H., Takeyasu, K., Haraguchi, T., and Hiraoka, Y. (2012). Lamin B receptor recognizes specific modifications of histone H4 in heterochromatin formation. J Biol Chem 287, 42654-42663. doi: 10.1074/jbc.M112.397950.
48. Ho, C.Y., and Lammerding, J. (2012). Lamins at a glance. J Cell Sci 125, 2087- 2093. doi: 10.1242/jcs.087288.
49. Hogarth, C., Itman, C., Jans, D.A., and Loveland, K.L. (2005). Regulated nucleocytoplasmic transport in spermatogenesis: a driver of cellular differentiation? Bioessays 27, 1011-1025.
50. Horn, H.F., Kim, D.I., Wright, G.D., Wong, E.S., Stewart, C.L., Burke, B., and Roux, K.J. (2013). A mammalian KASH domain protein coupling meiotic chromosomes to the cytoskeleton. J Cell Biol 202, 1023-1039. doi: 10.1083/jcb.201304004.
51. Hu, T., and Gerace, L. (1998). cDNA cloning and analysis of the expression of nucleoporin p45. Gene 221, 245-253.
52. Ikegami, K., Egelhofer, T.A., Strome, S., and Lieb, J.D. (2010). Caenorhabditis elegans chromosome arms are anchored to the nuclear membrane via discontinuous association with LEM-2. Genome Biol 11, R120. doi: 10.1186/gb-2010-11-12-r120.
53. Ikegami, K., and Lieb, J.D. (2013). Integral nuclear pore proteins bind to Pol IIItranscribed genes and are required for Pol III transcript processing in C. elegans. Mol Cell 51, 840-849. doi: S1097-2765(13)00574-1 [pii] 10.1016/j.molcel.2013.08.001.
54. Ishii, K., Arib, G., Lin, C., Van Houwe, G., and Laemmli, U.K. (2002). Chromatin boundaries in budding yeast: the nuclear pore connection. Cell 109, 551- 562.
55. Kalverda, B., and Fornerod, M. (2010). Characterization of genome-nucleoporin interactions in Drosophila links chromatin insulators to the nuclear pore complex. Cell Cycle 9, 4812-4817. doi: 14328 [pii].
56. Kalverda, B., Pickersgill, H., Shloma, V.V., and Fornerod, M. (2010). Nucleoporins directly stimulate expression of developmental and cell-cycle genes inside the nucleoplasm. Cell 140, 360-371. doi: S0092- 8674(10)00012-7 [pii] 10.1016/j.cell.2010.01.011.
57. Kim, Y., Sharov, A.A., Mcdole, K., Cheng, M., Hao, H., Fan, C.M., Gaiano, N., Ko, M.S., and Zheng, Y. (2011). Mouse B-type lamins are required for proper organogenesis but not by embryonic stem cells. Science 334, 1706-1710. doi: 10.1126/science.1211222.
58. Kind, J., Pagie, L., Ortabozkoyun, H., Boyle, S., De Vries, S.S., Janssen, H., Amendola, M., Nolen, L.D., Bickmore, W.A., and Van Steensel, B. (2013). Single-cell dynamics of genome-nuclear lamina interactions. Cell 153, 178-192. doi: 10.1016/j.cell.2013.02.028.
59. Kind, J., and Van Steensel, B. (2014). Stochastic genome-nuclear lamina interactions: modulating roles of Lamin A and BAF. Nucleus 5, 124-130. doi: 10.4161/nucl.28825.
60. Kohwi, M., Lupton, J.R., Lai, S.L., Miller, M.R., and Doe, C.Q. (2013). Developmentally regulated subnuclear genome reorganization restricts neural progenitor competence in Drosophila. Cell 152, 97-108. doi: 10.1016/j.cell.2012.11.049.
61. Kolb, T., Maass, K., Hergt, M., Aebi, U., and Herrmann, H. (2011). Lamin A and lamin C form homodimers and coexist in higher complex forms both in the nucleoplasmic fraction and in the lamina of cultured human cells. Nucleus 2, 425-433. doi: http://dx.doi.org/10.4161/nucl.2.5.17765 10.4161/nucl.2.5.17765.
62. Korfali, N., Wilkie, G.S., Swanson, S.K., Srsen, V., Batrakou, D.G., Fairley, E.A., Malik, P., Zuleger, N., Goncharevich, A., De Las Heras, J., Kelly, D.A., Kerr, A.R., Florens, L., and Schirmer, E.C. (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. doi: 10.1074/mcp.M110.002915.
63. Korfali, N., Wilkie, G.S., Swanson, S.K., Srsen, V., De Las Heras, J., Batrakou, D.G., Malik, P., Zuleger, N., Kerr, A.R., Florens, L., and Schirmer, E.C. (2012). The nuclear envelope proteome differs notably between tissues. Nucleus 3, 552-564. doi: 10.4161/nucl.22257.
64. Krull, S., Dorries, J., Boysen, B., Reidenbach, S., Magnius, L., Norder, H., Thyberg, J., and Cordes, V.C. (2010). Protein Tpr is required for establishing nuclear pore-associated zones of heterochromatin exclusion. EMBO J 29, 1659-1673. doi: 10.1038/emboj.2010.54.
65. Kumaran, R.I., and Spector, D.L. (2008). A genetic locus targeted to the nuclear periphery in living cells maintains its transcriptional competence. J Cell Biol 180, 51-65. doi: 10.1083/jcb.200706060.
66. Kumaran, R.I., Thakar, R., and Spector, D.L. (2008). Chromatin dynamics and gene positioning. Cell 132, 929-934. doi: 10.1016/j.cell.2008.03.004.
67. Legartova, S., Stixova, L., Laur, O., Kozubek, S., Sehnalova, P., and Bartova, E. (2014). Nuclear structures surrounding internal lamin invaginations. J Cell Biochem 115, 476-487. doi: 10.1002/jcb.24681.
68. Liang, Y., Franks, T.M., Marchetto, M.C., Gage, F.H., and Hetzer, M.W. (2013). Dynamic association of NUP98 with the human genome. PLoS Genet 9, e1003308. doi: 10.1371/journal.pgen.1003308 PGENETICS-D-12-01273 [pii].
69. Light, W.H., Brickner, D.G., Brand, V.R., and Brickner, J.H. (2010). Interaction of a DNA zip code with the nuclear pore complex promotes H2A.Z incorporation and INO1 transcriptional memory. Mol Cell 40, 112-125. doi: S1097-2765(10)00709-4 [pii] 10.1016/j.molcel.2010.09.007.
70. Light, W.H., Freaney, J., Sood, V., Thompson, A., D'urso, A., Horvath, C.M., and Brickner, J.H. (2013). A conserved role for human Nup98 in altering chromatin structure and promoting epigenetic transcriptional memory. PLoS Biol 11, e1001524. doi: 10.1371/journal.pbio.1001524 PBIOLOGY-D-12-03595 [pii].
71. Lombardi, M.L., and Lammerding, J. (2011). Keeping the LINC: the importance of nucleocytoskeletal coupling in intracellular force transmission and cellular function. Biochem Soc Trans 39, 1729-1734. doi: 10.1042/BST20110686.
72. Luperchio, T.R., Wong, X., and Reddy, K.L. (2014). Genome regulation at the peripheral zone: lamina associated domains in development and disease. Curr Opin Genet Dev 25, 50-61. doi: 10.1016/j.gde.2013.11.021.
73. Lupu, F., Alves, A., Anderson, K., Doye, V., and Lacy, E. (2008). Nuclear pore composition regulates neural stem/progenitor cell differentiation in the mouse embryo. Dev Cell 14, 831-842.
74. Luthra, R., Kerr, S.C., Harreman, M.T., Apponi, L.H., Fasken, M.B., Ramineni, S., Chaurasia, S., Valentini, S.R., and Corbett, A.H. (2007). Actively transcribed GAL genes can be physically linked to the nuclear pore by the SAGA chromatin modifying complex. J Biol Chem 282, 3042-3049.
75. Makatsori, D., Kourmouli, N., Polioudaki, H., Shultz, L.D., Mclean, K., Theodoropoulos, P.A., Singh, P.B., and Georgatos, S.D. (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. doi: 10.1074/jbc.M313606200.
76. Malik, P., Korfali, N., Srsen, V., Lazou, V., Batrakou, D.G., Zuleger, N., Kavanagh, D.M., Wilkie, G.S., Goldberg, M.W., and Schirmer, E.C. (2010). Cell-specific and lamin-dependent targeting of novel transmembrane proteins in the nuclear envelope. Cell Mol Life Sci 67, 1353-1369. doi: 10.1007/s00018-010-0257-2.
77. Mattout, A., and Meshorer, E. (2010). Chromatin plasticity and genome organization in pluripotent embryonic stem cells. Curr Opin Cell Biol 22, 334-341. doi: 10.1016/j.ceb.2010.02.001.
78. Meier, I., and Brkljacic, J. (2009). The nuclear pore and plant development. Curr Opin Plant Biol 12, 87-95.
79. Mendjan, S., Taipale, M., Kind, J., Holz, H., Gebhardt, P., Schelder, M., Vermeulen, M., Buscaino, A., Duncan, K., Mueller, J., Wilm, M., Stunnenberg, H.G., Saumweber, H., and Akhtar, A. (2006). Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila. Mol Cell 21, 811-823.
80. Meshorer, E., Yellajoshula, D., George, E., Scambler, P.J., Brown, D.T., and Misteli, T. (2006). Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell 10, 105-116. doi: 10.1016/j.devcel.2005.10.017.
81. Moir, R.D., Spann, T.P., Lopez-Soler, R.I., Yoon, M., Goldman, A.E., Khuon, S., and Goldman, R.D. (2000a). Review: the dynamics of the nuclear lamins during the cell cycle-relationship between structure and function. J Struct Biol 129, 324-334. doi: 10.1006/jsbi.2000.4251.
82. Moir, R.D., Yoon, M., Khuon, S., and Goldman, R.D. (2000b). Nuclear lamins A and B1: different pathways of assembly during nuclear envelope formation in living cells. J Cell Biol 151, 1155-1168.
83. Morimoto, A., Shibuya, H., Zhu, X., Kim, J., Ishiguro, K., Han, M., and Watanabe, Y. (2012). A conserved KASH domain protein associates with telomeres, SUN1, and dynactin during mammalian meiosis. J Cell Biol 198, 165-172. doi: 10.1083/jcb.201204085.
84. Murawala, P., Tripathi, M.M., Vyas, P., Salunke, A., and Joseph, J. (2009). Nup358 interacts with APC and plays a role in cell polarization. J Cell Sci 122, 3113-3122. doi: 10.1242/jcs.037523.
85. Neumann, S., and Noegel, A.A. (2014). Nesprins in cell stability and migration. Adv Exp Med Biol 773, 491-504. doi: 10.1007/978-1-4899-8032-8_22.
86. Padeken, J., and Heun, P. (2014). Nucleolus and nuclear periphery: velcro for heterochromatin. Curr Opin Cell Biol 28, 54-60. doi: 10.1016/j.ceb.2014.03.001.
87. Padmakumar, V.C., Libotte, T., Lu, W., Zaim, H., Abraham, S., Noegel, A.A., Gotzmann, J., Foisner, R., and Karakesisoglou, I. (2005). The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope. J Cell Sci 118, 3419-3430. doi: 10.1242/jcs.02471.
88. Parrott, B.B., Chiang, Y., Hudson, A., Sarkar, A., Guichet, A., and Schulz, C. (2011). Nucleoporin98-96 function is required for transit amplification divisions in the germ line of Drosophila melanogaster. PLoS One 6, e25087. doi: 10.1371/journal.pone.0025087.
89. Pascual-Garcia, P., Govind, C.K., Queralt, E., Cuenca-Bono, B., Llopis, A., Chavez, S., Hinnebusch, A.G., and Rodriguez-Navarro, S. (2008). Sus1 is recruited to coding regions and functions during transcription elongation in association with SAGA and TREX2. Genes Dev 22, 2811-2822. doi: 22/20/2811 [pii] 10.1101/gad.483308.
90. Pascual-Garcia, P., Jeong, J., and Capelson, M. (2014). Nucleoporin Nup98 Associates with Trx/MLL and NSL Histone-Modifying Complexes and Regulates Hox Gene Expression. Cell Rep. doi: 10.1016/j.celrep.2014.09.002.
91. Perez-Terzic, C., Behfar, A., Mery, A., Van Deursen, J.M., Terzic, A., and Puceat, M. (2003). Structural adaptation of the nuclear pore complex in stem cell-derived cardiomyocytes. Circ Res 92, 444-452. doi: 10.1161/01.RES.0000059415.25070.54.
92. Peric-Hupkes, D., Meuleman, W., Pagie, L., Bruggeman, S.W., Solovei, I., Brugman, W., Graf, S., Flicek, P., Kerkhoven, R.M., Van Lohuizen, M., Reinders, M., Wessels, L., and Van Steensel, B. (2010). Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol Cell 38, 603-613. doi: 10.1016/j.molcel.2010.03.016.
93. Peric-Hupkes, D., and Van Steensel, B. (2010). Role of the nuclear lamina in genome organization and gene expression. Cold Spring Harb Symp Quant Biol 75, 517-524. doi: 10.1101/sqb.2010.75.014.
94. Prokocimer, M., Davidovich, M., Nissim-Rafinia, M., Wiesel-Motiuk, N., Bar, D.Z., Barkan, R., Meshorer, E., and Gruenbaum, Y. (2009). Nuclear lamins: key regulators of nuclear structure and activities. J Cell Mol Med 13, 1059- 1085. doi: 10.1111/j.1582-4934.2008.00676.x.
95. Ptak, C., Aitchison, J.D., and Wozniak, R.W. (2014). The multifunctional nuclear pore complex: a platform for controlling gene expression. Curr Opin Cell Biol 28, 46-53. doi: 10.1016/j.ceb.2014.02.001.
96. Rabut, G., Doye, V., and Ellenberg, J. (2004). Mapping the dynamic organization of the nuclear pore complex inside single living cells. Nat Cell Biol 6, 1114- 1121.
97. Raices, M., and D'angelo, M.A. (2012). Nuclear pore complex composition: a new regulator of tissue-specific and developmental functions. Nat Rev Mol Cell Biol 13, 687-699. doi: nrm3461 [pii] 10.1038/nrm3461.
98. Randles, K.N., Lam Le, T., Sewry, C.A., Puckelwartz, M., Furling, D., Wehnert, M., Mcnally, E.M., and Morris, G.E. (2010). Nesprins, but not sun proteins, switch isoforms at the nuclear envelope during muscle development. Dev Dyn 239, 998-1009. doi: 10.1002/dvdy.22229.
99. Razafsky, D., Zang, S., and Hodzic, D. (2011). UnLINCing the nuclear envelope: towards an understanding of the physiological significance of nuclear positioning. Biochem Soc Trans 39, 1790-1794. doi: 10.1042/BST20110660.
100. Razafsky, D.S., Ward, C.L., Kolb, T., and Hodzic, D. (2013). Developmental regulation of linkers of the nucleoskeleton to the cytoskeleton during mouse postnatal retinogenesis. Nucleus 4, 399-409. doi: 10.4161/nucl.26244.
101. Reddy, K.L., and Singh, H. (2008). Using molecular tethering to analyze the role of nuclear compartmentalization in the regulation of mammalian gene activity. Methods 45, 242-251. doi: 10.1016/j.ymeth.2008.06.013.
102. Reddy, K.L., Zullo, J.M., Bertolino, E., and Singh, H. (2008). Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature.
103. Reik, W. (2007). Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425-432. doi: 10.1038/nature05918.
104. Rober, R.A., Weber, K., and Osborn, M. (1989). Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: a developmental study. Development 105, 365-378.
105. Rodriguez-Navarro, S., Fischer, T., Luo, M.J., Antunez, O., Brettschneider, S., Lechner, J., Perez-Ortin, J.E., Reed, R., and Hurt, E. (2004). Sus1, a functional component of the SAGA histone acetylase complex and the nuclear pore-associated mRNA export machinery. Cell 116, 75-86.
106. Rougemaille, M., Dieppois, G., Kisseleva-Romanova, E., Gudipati, R.K., Lemoine, S., Blugeon, C., Boulay, J., Jensen, T.H., Stutz, F., Devaux, F., and Libri, D. (2008). THO/Sub2p functions to coordinate 3'-end processing with gene-nuclear pore association. Cell 135, 308-321.
107. Roux, K.J., Crisp, M.L., Liu, Q., Kim, D., Kozlov, S., Stewart, C.L., and Burke, B. (2009). Nesprin 4 is an outer nuclear membrane protein that can induce kinesin-mediated cell polarization. Proc Natl Acad Sci U S A 106, 2194- 2199. doi: 10.1073/pnas.0808602106.
108. Ruben, G.J., Kirkland, J.G., Macdonough, T., Chen, M., Dubey, R.N., Gartenberg, M.R., and Kamakaka, R.T. (2011). Nucleoporin mediated nuclear positioning and silencing of HMR. PLoS One 6, e21923. doi: 10.1371/journal.pone.0021923 PONE-D-11-07429 [pii].
109. Sato, A., Isaac, B., Phillips, C.M., Rillo, R., Carlton, P.M., Wynne, D.J., Kasad, R.A., and Dernburg, A.F. (2009). Cytoskeletal forces span the nuclear envelope to coordinate meiotic chromosome pairing and synapsis. Cell 139, 907-919. doi: 10.1016/j.cell.2009.10.039.
110. Schirmer, E.C., Florens, L., Guan, T., Yates, J.R., 3rd, and Gerace, L. (2003). Nuclear membrane proteins with potential disease links found by subtractive proteomics. Science 301, 1380-1382. doi: 10.1126/science.1088176.
111. Schmid, M., Arib, G., Laemmli, C., Nishikawa, J., Durussel, T., and Laemmli, U.K. (2006). Nup-PI: the nucleopore-promoter interaction of genes in yeast. Mol Cell 21, 379-391.
112. Schneider, R., and Grosschedl, R. (2007). Dynamics and interplay of nuclear architecture, genome organization, and gene expression. Genes Dev 21, 3027-3043.
113. Schuler, E., Lin, F., and Worman, H.J. (1994). Characterization of the human gene encoding LBR, an integral protein of the nuclear envelope inner membrane. J Biol Chem 269, 11312-11317.
114. Senger, S., Csokmay, J., Akbar, T., Jones, T.I., Sengupta, P., and Lilly, M.A. (2011). The nucleoporin Seh1 forms a complex with Mio and serves an essential tissue-specific function in Drosophila oogenesis. Development 138, 2133-2142. doi: 10.1242/dev.057372.
115. Sharma, M., Jamieson, C., Johnson, M., Molloy, M.P., and Henderson, B.R. (2012). Specific armadillo repeat sequences facilitate beta-catenin nuclear transport in live cells via direct binding to nucleoporins Nup62, Nup153, and RanBP2/Nup358. J Biol Chem 287, 819-831. doi: 10.1074/jbc.M111.299099.
116. Sharma, M., Johnson, M., Brocardo, M., Jamieson, C., and Henderson, B.R. (2014). Wnt signaling proteins associate with the nuclear pore complex: implications for cancer. Adv Exp Med Biol 773, 353-372. doi: 10.1007/978- 1-4899-8032-8_16.
117. Shimi, T., Pfleghaar, K., Kojima, S., Pack, C.G., Solovei, I., Goldman, A.E., Adam, S.A., Shumaker, D.K., Kinjo, M., Cremer, T., and Goldman, R.D. (2008). The A- and B-type nuclear lamin networks: microdomains involved in chromatin organization and transcription. Genes Dev 22, 3409-3421. doi: 10.1101/gad.1735208.
118. Shitashige, M., Satow, R., Honda, K., Ono, M., Hirohashi, S., and Yamada, T. (2008). Regulation of Wnt signaling by the nuclear pore complex. Gastroenterology 134, 1961-1971, 1971 e1961-1964. doi: 10.1053/j.gastro.2008.03.010.
119. Simpson, J.G., and Roberts, R.G. (2008). Patterns of evolutionary conservation in the nesprin genes highlight probable functionally important protein domains and isoforms. Biochem Soc Trans 36, 1359-1367. doi: 10.1042/BST0361359.
120. Smitherman, M., Lee, K., Swanger, J., Kapur, R., and Clurman, B.E. (2000). Characterization and targeted disruption of murine Nup50, a p27(Kip1)- interacting component of the nuclear pore complex. Mol Cell Biol 20, 5631-5642.
121. Snider, N.T., and Omary, M.B. (2014). Post-translational modifications of intermediate filament proteins: mechanisms and functions. Nat Rev Mol Cell Biol 15, 163-177. doi: 10.1038/nrm3753.
122. Solovei, I., Kreysing, M., Lanctot, C., Kosem, S., Peichl, L., Cremer, T., Guck, J., and Joffe, B. (2009). Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell 137, 356-368. doi: 10.1016/j.cell.2009.01.052.
123. Solovei, I., Wang, A.S., Thanisch, K., Schmidt, C.S., Krebs, S., Zwerger, M., Cohen, T.V., Devys, D., Foisner, R., Peichl, L., Herrmann, H., Blum, H., Engelkamp, D., Stewart, C.L., Leonhardt, H., and Joffe, B. (2013). LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 152, 584-598. doi: 10.1016/j.cell.2013.01.009.
124. Sood, V., and Brickner, J.H. (2014). Nuclear pore interactions with the genome. Curr Opin Genet Dev 25, 43-49. doi: 10.1016/j.gde.2013.11.018.
125. Stewart, C., and Burke, B. (1987). Teratocarcinoma stem cells and early mouse embryos contain only a single major lamin polypeptide closely resembling lamin B. Cell 51, 383-392.
126. Stierle, V., Couprie, J., Ostlund, C., Krimm, I., Zinn-Justin, S., Hossenlopp, P., Worman, H.J., Courvalin, J.C., and Duband-Goulet, I. (2003). The carboxyl-terminal region common to lamins A and C contains a DNA binding domain. Biochemistry 42, 4819-4828. doi: 10.1021/bi020704g.
127. Sullivan, T., Escalante-Alcalde, D., Bhatt, H., Anver, M., Bhat, N., Nagashima, K., Stewart, C.L., and Burke, B. (1999). Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 147, 913-920.
128. Taddei, A., Van Houwe, G., Hediger, F., Kalck, V., Cubizolles, F., Schober, H., and Gasser, S.M. (2006). Nuclear pore association confers optimal expression levels for an inducible yeast gene. Nature 441, 774-778.
129. Tan-Wong, S.M., Wijayatilake, H.D., and Proudfoot, N.J. (2009). Gene loops function to maintain transcriptional memory through interaction with the nuclear pore complex. Genes Dev 23, 2610-2624. doi: 23/22/2610 [pii] 10.1101/gad.1823209.
130. Taniura, H., Glass, C., and Gerace, L. (1995). A chromatin binding site in the tail domain of nuclear lamins that interacts with core histones. J Cell Biol 131, 33-44.
131. Toyama, B.H., Savas, J.N., Park, S.K., Harris, M.S., Ingolia, N.T., Yates, J.R., 3rd, and Hetzer, M.W. (2013). Identification of long-lived proteins reveals exceptional stability of essential cellular structures. Cell 154, 971-982. doi: S0092-8674(13)00945-8 [pii] 10.1016/j.cell.2013.07.037.
132. Trichet, V., Shkolny, D., Dunham, I., Beare, D., and Mcdermid, H.E. (1999). Mapping and complex expression pattern of the human NPAP60L nucleoporin gene. Cytogenet Cell Genet 85, 221-226. doi: 15297.
133. Ueda, J., Maehara, K., Mashiko, D., Ichinose, T., Yao, T., Hori, M., Sato, Y., Kimura, H., Ohkawa, Y., and Yamagata, K. (2014). Heterochromatin dynamics during the differentiation process revealed by the DNA methylation reporter mouse, MethylRO. Stem Cell Reports 2, 910-924. doi: 10.1016/j.stemcr.2014.05.008.
134. Ulbert, S., Platani, M., Boue, S., and Mattaj, I.W. (2006). Direct membrane protein-DNA interactions required early in nuclear envelope assembly. J Cell Biol 173, 469-476. doi: 10.1083/jcb.200512078.
135. Van Bortle, K., and Corces, V.G. (2012). Nuclear organization and genome function. Annu Rev Cell Dev Biol 28, 163-187. doi: 10.1146/annurevcellbio- 101011-155824.
136. Van De Vosse, D.W., Wan, Y., Lapetina, D.L., Chen, W.M., Chiang, J.H., Aitchison, J.D., and Wozniak, R.W. (2013). A role for the nucleoporin Nup170p in chromatin structure and gene silencing. Cell 152, 969-983. doi: S0092-8674(13)00141-4 [pii] 10.1016/j.cell.2013.01.049.
137. Van De Vosse, D.W., Wan, Y., Wozniak, R.W., and Aitchison, J.D. (2011). Role of the nuclear envelope in genome organization and gene expression. Wiley Interdiscip Rev Syst Biol Med 3, 147-166. doi: 10.1002/wsbm.101.
138. Vaquerizas, J.M., Suyama, R., Kind, J., Miura, K., Luscombe, N.M., and Akhtar, A. (2010). Nuclear pore proteins nup153 and megator define transcriptionally active regions in the Drosophila genome. PLoS Genet 6, e1000846. doi: 10.1371/journal.pgen.1000846.
139. Voronina, E., and Seydoux, G. (2010). The C. elegans homolog of nucleoporin Nup98 is required for the integrity and function of germline P granules. Development 137, 1441-1450. doi: 10.1242/dev.047654.
140. Wen, B., Wu, H., Loh, Y.H., Briem, E., Daley, G.Q., and Feinberg, A.P. (2012). Euchromatin islands in large heterochromatin domains are enriched for CTCF binding and differentially DNA-methylated regions. BMC Genomics 13, 566. doi: 10.1186/1471-2164-13-566.
141. Wen, B., Wu, H., Shinkai, Y., Irizarry, R.A., and Feinberg, A.P. (2009). Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nat Genet 41, 246-250. doi: 10.1038/ng.297.
142. Wente, S.R., and Rout, M.P. (2010). The nuclear pore complex and nuclear transport. Cold Spring Harb Perspect Biol 2, a000562. doi: cshperspect.a000562 [pii] 10.1101/cshperspect.a000562.
143. Wilhelmsen, K., Litjens, S.H., Kuikman, I., Tshimbalanga, N., Janssen, H., Van Den Bout, I., Raymond, K., and Sonnenberg, A. (2005). Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J Cell Biol 171, 799-810. doi: 10.1083/jcb.200506083.
144. Wilkie, G.S., Korfali, N., Swanson, S.K., Malik, P., Srsen, V., Batrakou, D.G., De Las Heras, J., Zuleger, N., Kerr, A.R., Florens, L., and Schirmer, E.C. (2011). Several novel nuclear envelope transmembrane proteins identified in skeletal muscle have cytoskeletal associations. Mol Cell Proteomics 10, M110 003129. doi: 10.1074/mcp.M110.003129.
145. Woglar, A., and Jantsch, V. (2014). Chromosome movement in meiosis I prophase of Caenorhabditis elegans. Chromosoma 123, 15-24. doi: 10.1007/s00412-013-0436-7.
146. Worman, H.J. (2005). Components of the nuclear envelope and their role in human disease. Novartis Found Symp 264, 35-42; discussion 42-50, 227- 230.
147. Worman, H.J., Lazaridis, I., and Georgatos, S.D. (1988a). Nuclear lamina heterogeneity in mammalian cells. Differential expression of the major lamins and variations in lamin B phosphorylation. J Biol Chem 263, 12135- 12141.
148. Worman, H.J., Yuan, J., Blobel, G., and Georgatos, S.D. (1988b). A lamin B receptor in the nuclear envelope. Proc Natl Acad Sci U S A 85, 8531- 8534.
149. Wu, R., Terry, A.V., Singh, P.B., and Gilbert, D.M. (2005). Differential subnuclear localization and replication timing of histone H3 lysine 9 methylation states. Mol Biol Cell 16, 2872-2881. doi: 10.1091/mbc.E04-11-0997.
150. Xu, S., and Powers, M.A. (2009). Nuclear pore proteins and cancer. Semin Cell Dev Biol 20, 620-630. doi: S1084-9521(09)00041-X [pii] 10.1016/j.semcdb.2009.03.003.
151. Xylourgidis, N., and Fornerod, M. (2009). Acting out of character: regulatory roles of nuclear pore complex proteins. Dev Cell 17, 617-625. doi: 10.1016/j.devcel.2009.10.015.
152. Yang, J., Cai, N., Yi, F., Liu, G.H., Qu, J., and Izpisua Belmonte, J.C. (2014). Gating pluripotency via nuclear pores. Trends Mol Med 20, 1-7. doi: 10.1016/j.molmed.2013.10.003.
153. Yang, L., Munck, M., Swaminathan, K., Kapinos, L.E., Noegel, A.A., and Neumann, S. (2013). Mutations in LMNA modulate the lamin A--Nesprin-2 interaction and cause LINC complex alterations. PLoS One 8, e71850. doi: 10.1371/journal.pone.0071850.
154. Ye, Q., Callebaut, I., Pezhman, A., Courvalin, J.C., and Worman, H.J. (1997). Domain-specific interactions of human HP1-type chromodomain proteins and inner nuclear membrane protein LBR. J Biol Chem 272, 14983-14989.
155. Ye, Q., and Worman, H.J. (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.
156. Zhang, Q., Ragnauth, C.D., Skepper, J.N., Worth, N.F., Warren, D.T., Roberts, R.G., Weissberg, P.L., Ellis, J.A., and Shanahan, C.M. (2005). Nesprin-2 is a multi-isomeric protein that binds lamin and emerin at the nuclear envelope and forms a subcellular network in skeletal muscle. J Cell Sci 118, 673-687. doi: 10.1242/jcs.01642.
157. Zhang, X., Chen, S., Yoo, S., Chakrabarti, S., Zhang, T., Ke, T., Oberti, C., Yong, S.L., Fang, F., Li, L., De La Fuente, R., Wang, L., Chen, Q., and Wang, Q.K. (2008). Mutation in nuclear pore component NUP155 leads to atrial fibrillation and early sudden cardiac death. Cell 135, 1017-1027.
158. Zuleger, N., Boyle, S., Kelly, D.A., De Las Heras, J.I., Lazou, V., Korfali, N., Batrakou, D.G., Randles, K.N., Morris, G.E., Harrison, D.J., Bickmore, W.A., and Schirmer, E.C. (2013). Specific nuclear envelope transmembrane proteins can promote the location of chromosomes to and from the nuclear periphery. Genome Biol 14, R14. doi: 10.1186/gb-2013- 14-2-r14.
159. Zullo, J.M., Demarco, I.A., Pique-Regi, R., Gaffney, D.J., Epstein, C.B., Spooner, C.J., Luperchio, T.R., Bernstein, B.E., Pritchard, J.K., Reddy, K.L., and Singh, H. (2012). DNA sequence-dependent compartmentalization and silencing of chromatin at the nuclear lamina. Cell 149, 1474-1487. doi: 10.1016/j.cell.2012.04.035.
160. Zuo, B., Yang, J., Wang, F., Wang, L., Yin, Y., Dan, J., Liu, N., and Liu, L. (2012). Influences of lamin A levels on induction of pluripotent stem cells. Biol Open 1, 1118-1127. doi: 10.1242/bio.20121586.