Nuclear envelope influences on cell-cycle progression

Biochemical Society Transactions

Volumn 39, Issue 6, 2011, Pages 1742-1746

  Srsen, Vlastimil ^a   Nadia, Korfali ^a   Schirmer, Eric C ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cell cycle; Cell polarity; Inner nuclear membrane; Nuclear envelope; Retinoblastoma protein; Tmem53

Indexed keywords

EMERIN; KARYOPHERIN BETA; LAMIN A; MEMBRANE PROTEIN; PROTEIN P53; RETINOBLASTOMA PROTEIN; SMAD PROTEIN; TRANSCRIPTION FACTOR E2F; TRANSCRIPTION FACTOR IIH; TRANSFORMING GROWTH FACTOR BETA;

CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL NUCLEUS MEMBRANE; CELL PROLIFERATION; CONFERENCE PAPER; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION;

ANIMALS; CELL CYCLE; HUMANS; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; ORGAN SPECIFICITY; TRANSCRIPTION FACTORS;

EID: 81855217990     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20110656     Document Type: Conference Paper

References (47)

1. Suntharalingam, M. and Wente, S.R. (2003) Peering through the pore: nuclear pore complex structure, assembly, and function. Dev. Cell 4, 775-789 (Pubitemid 36676031)
2. Stewart, C.L., Roux, K.J. and Burke, B. (2007) Blurring the boundary: the nuclear envelope extends its reach. Science 318, 1408-1412 (Pubitemid 350208920)
3. Hetzer, M.W., Walther, T.C. and Mattaj, I.W. (2005) Pushing the envelope: structure, function, and dynamics of the nuclear periphery. Annu. Rev. Cell. Dev. Biol. 21, 347-380 (Pubitemid 41740639)
4. Voeltz, G.K., Prinz, W.A., Shibata, Y., Rist, J.M. and Rapoport, T.A. (2006) A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124, 573-586 (Pubitemid 43199442)
5. Starr, D.A. and Han, M. (2002) Role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science 298, 406-409 (Pubitemid 35176347)
6. 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. et al. (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
7. 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
8. 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
9. Mattout-Drubezki, A. and Gruenbaum, Y. (2003) Dynamic interactions of nuclear lamina proteins with chromatin and transcriptional machinery. Cell. Mol. Life Sci. 60, 2053-2063 (Pubitemid 37357416)
10. Schirmer, E.C. and Foisner, R. (2007) Proteins that associate with lamins: many faces, many functions. Exp. Cell Res. 313, 2167-2179 (Pubitemid 46842977)
11. Foisner, R., Aebi, U., Bonne, G., Gruenbaum, Y. and Novelli, G. (2007) 141st ENMC International Workshop inaugural meeting of the EURO-Laminopathies project "Nuclear Envelope-linked Rare Human Diseases: From Molecular Pathophysiology towards Clinical Applications", 10-12 March 2006, Naarden, The Netherlands. Neuromuscul. Disord. 17, 655-660 (Pubitemid 47030918)
12. Worman, H.J. and Bonne, G. (2007) "Laminopathies": a wide spectrum of human diseases. Exp. Cell Res. 313, 2121-2133 (Pubitemid 46850729)
13. Gerace, L. and Blobel, G. (1980) The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell 19, 277-287 (Pubitemid 10154232)
14. Peter, M., Nakagawa, J., Doree, M., Labbe, J.C. and Nigg, E.A. (1990) In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase. Cell 61, 591-602
15. Heald, R. and McKeon, F. (1990) Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 61, 579-589
16. Belgareh, N., Rabut, G., Bai, S.W., van Overbeek, M., Beaudouin, J., Daigle, N., Zatsepina, O.V., Pasteau, F., Labas, V., Fromont-Racine, M. et al. (2001) An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells. J. Cell Biol. 154, 1147-1160 (Pubitemid 34286193)
17. Ohba, T., Nakamura, M., Nishitani, H. and Nishimoto, T. (1999) Self-organization of microtubule asters induced in Xenopus egg extracts by GTP-bound Ran. Science 284, 1356-1358 (Pubitemid 29289661)
18. Wiese, C., Wilde, A., Moore, M.S., Adam, S.A., Merdes, A. and Zheng, Y. (2001) Role of importin-β in coupling Ran to downstream targets in microtubule assembly. Science 291, 653-656 (Pubitemid 32150424)
19. Buch, C., Lindberg, R., Figueroa, R., Gudise, S., Onischenko, E. and 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
20. Tsai, M.Y., Wang, S., Heidinger, J.M., Shumaker, D.K., Adam, S.A., Goldman, R.D. and Zheng, Y. (2006) A mitotic lamin B matrix induced by RanGTP required for spindle assembly. Science 311, 1887-1893
21. 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 (Pubitemid 43042628)
22. McGee, M.D., Stagljar, I. and Starr, D.A. (2009) KDP-1 is a nuclear envelope KASH protein required for cell-cycle progression. J. Cell Sci. 122, 2895-2905
23. Ozaki, T., Saijo, M., Murakami, K., Enomoto, H., Taya, Y. and Sakiyama, S. (1994) Complex formation between lamin A and the retinoblastoma gene product: identification of the domain on lamin A required for its interaction. Oncogene 9, 2649-2653 (Pubitemid 24254041)
24. Markiewicz, E., Dechat, T., Foisner, R., Quinlan, R. and Hutchison, C. (2002) Lamin A/C binding protein LAP2α is required for nuclear anchorage of retinoblastoma protein. Mol. Biol. Cell. 13, 4401-4413 (Pubitemid 35471194)
25. Genovese, C., Trani, D., Caputi, M. and Claudio, P.P. (2006) Cell cycle control and beyond: emerging roles for the retinoblastoma gene family. Oncogene 25, 5201-5209 (Pubitemid 44299078)
26. Templeton, D.J. (1992) Nuclear binding of purified retinoblastoma gene product is determined by cell cycle-regulated phosphorylation. Mol. Cell. Biol. 12, 435-443
27. 1/S cyclin-dependent kinases. J. Biol. Chem. 272, 12738-12746
28. Johnson, B.R., Nitta, R.T., Frock, R.L., Mounkes, L., Barbie, D.A., Stewart, C.L., Harlow, E. and Kennedy, B.K. (2004) A-type lamins regulate retinoblastoma protein function by promoting subnuclear localization and preventing proteasomal degradation. Proc. Natl. Acad. Sci. U.S.A. 101, 9677-9682 (Pubitemid 38869295)
29. Dorner, D., Vlcek, S., Foeger, N., Gajewski, A., Makolm, C., Gotzmann, J., Hutchison, C.J. and Foisner, R. (2006) Lamina-associated polypeptide 2α regulates cell cycle progression and differentiation via the retinoblastoma-E2F pathway. J. Cell Biol. 173, 83-93
30. Pekovic, V., Harborth, J., Broers, J.L., Ramaekers, F.C., van Engelen, B., Lammens, M., von Zglinicki, T., Foisner, R., Hutchison, C. and Markiewicz, E. (2007) Nucleoplasmic LAP2α-lamin A complexes are required to maintain a proliferative state in human fibroblasts. J. Cell Biol. 176, 163-172 (Pubitemid 46143257)
31. Naetar, N., Korbei, B., Kozlov, S., Kerenyi, M.A., Dorner, D., Kral, R., Gotic, I., Fuchs, P., Cohen, T.V., Bittner, R. et al. (2008) Loss of nucleoplasmic LAP2α-lamin A complexes causes erythroid and epidermal progenitor hyperproliferation. Nat. Cell Biol. 10, 1341-1348
32. Dechat, T., Gotzmann, J., Stockinger, A., Harris, C.A., Talle, M.A., Siekierka, J.J. and Foisner, R. (1998) Detergent-salt resistance of LAP2α in interphase nuclei and phosphorylation-dependent association with chromosomes early in nuclear assembly implies functions in nuclear structure dynamics. EMBO J. 17, 4887-4902 (Pubitemid 28377189)
33. Nili, E., Cojocaru, G.S., Kalma, Y., Ginsberg, D., Copeland, N.G., Gilbert, D.J., Jenkins, N.A., Berger, R., Shaklai, S., Amariglio, N. et al. (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 (Pubitemid 32998906)
34. Bengtsson, L. and Wilson, K.L. (2004) Multiple and surprising new functions for emerin, a nuclear membrane protein. Curr. Opin. Cell Biol. 16, 73-79 (Pubitemid 38368155)
35. Osada, S., Ohmori, S.Y. and Taira, M. (2003) XMAN1, an inner nuclear membrane protein, antagonizes BMP signaling by interacting with Smad1 in Xenopus embryos. Development 130, 1783-1794 (Pubitemid 36575906)
36. Pan, D., Estevez-Salmeron, L.D., Stroschein, S.L., Zhu, X., He, J., Zhou, S. and Luo, K. (2005) The integral inner nuclear membrane protein MAN1 physically interacts with the R-Smad proteins to repress signaling by the transforming growth factor-β superfamily of cytokines. J. Biol. Chem. 280, 15992-16001 (Pubitemid 40616723)
37. Ellis, J.A., Craxton, M., Yates, J.R. and Kendrick-Jones, J. (1998) Aberrant intracellular targeting and cell cycle-dependent phosphorylation of emerin contribute to the Emery-Dreifuss muscular dystrophy phenotype. J. Cell Sci. 111, 781-792 (Pubitemid 28163886)
38. Hirano, Y., Segawa, M., Ouchi, F.S., Yamakawa, Y., Furukawa, K., Takeyasu, K. and Horigome, T. (2005) Dissociation of emerin from barrier-to-autointegration factor is regulated through mitotic phosphorylation of emerin in a Xenopus egg cell-free system. J. Biol. Chem. 280, 39925-39933 (Pubitemid 41779127)
39. Korfali, N., Srsen, V., Waterfall, M., Batrakou, D.G., Pekovic, V., Hutchison, C.J. and Schirmer, E.C. (2011) A flow cytometry-based screen of nuclear envelope transmembrane proteins identifies NET4/Tmem53 as involved in stress-dependent cell cycle withdrawal. PLoS ONE 6, e18762
40. Wu, C., Orozco, C., Boyer, J., Leglise, M., Goodale, J., Batalov, S., Hodge, C.L., Haase, J., Janes, J., Huss, 3rd, J.W. and Su, A.I. (2009) BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol. 10, R130
41. Haffner, C., Dettmer, U., Weiler, T. and Haass, C. (2007) The Nicastrin-like protein Nicalin regulates assembly and stability of the Nicalin-nodal modulator (NOMO) membrane protein complex. J. Biol. Chem. 282, 10632-10638 (Pubitemid 47093442)
42. Markiewicz, E., Tilgner, K., Barker, N., van de Wetering, M., Clevers, H., Dorobek, M., Hausmanowa-Petrusewicz, I., Ramaekers, F.C., Broers, J.L., Blankesteijn, W.M. et al. (2006) The inner nuclear membrane protein emerin regulates β-catenin activity by restricting its accumulation in the nucleus. EMBO J. 25, 3275-3285 (Pubitemid 44141786)
43. Zarubin, T. and Han, J. (2005) Activation and signaling of the p38 MAP kinase pathway. Cell Res. 15, 11-18 (Pubitemid 41653958)
44. Bakay, M., Wang, Z., Melcon, G., Schiltz, L., Xuan, J., Zhao, P., Sartorelli, V., Seo, J., Pegoraro, E., Angelini, C. et al. (2006) Nuclear envelope dystrophies show a transcriptional fingerprint suggesting disruption of Rb-MyoD pathways in muscle regeneration. Brain 129, 996-1013
45. Melcon, G., Kozlov, S., Cutler, D.A., Sullivan, T., Hernandez, L., Zhao, P., Mitchell, S., Nader, G., Bakay, M., Rottman, J.N. et al. (2006) Loss of emerin at the nuclear envelope disrupts the Rb1/E2F and MyoD pathways during muscle regeneration. Hum. Mol. Genet. 15, 637-651 (Pubitemid 43205427)
46. Fairley, E., Riddell, A., Ellis, J. and Kendrick-Jones, J. (2002) The cell cycle dependent mislocalisation of emerin may contribute to the Emery-Dreifuss muscular dystrophy phenotype. J. Cell Sci. 115, 341-354
47. Liu, J., Lee, K., Segura-Totten, M., Neufeld, E., Wilson, K. and Gruenbaum, Y. (2003) MAN1 and emerin have overlapping function(s) essential for chromosome segregation and cell division in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 100, 4598-4603 (Pubitemid 36457776)