Synthesis, transport and incorporation into the nuclear envelope of A-type lamins and inner nuclear membrane proteins

Biochemical Society Transactions

Volumn 39, Issue 6, 2011, Pages 1758-1763

  González, Jose M ^a   Andrés, Vicente ^a  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

Author keywords

A type lamin; Inner nuclear membrane protein; Nuclear envelope; Nuclear envelope assembly and disassembly; Nuclear envelope turnover; Nuclear lamina

Indexed keywords

BARRIER TO AUTOINTEGRATION FACTOR; CYCLIN DEPENDENT KINASE 1; DNA; LAMIN A; LAMIN B; LAMIN C; MEMBRANE PROTEIN; NUCLEOPORIN;

CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL MIGRATION; CELL NUCLEUS MEMBRANE; CELL POLARITY; CONFERENCE PAPER; DNA DAMAGE; DNA REPLICATION; ENDOPLASMIC RETICULUM; INTERPHASE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT;

ANIMALS; HUMANS; LAMIN TYPE A; MEMBRANE PROTEINS; MITOSIS; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; PROTEIN TRANSPORT;

MAMMALIA;

EID: 81855220924     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20110653     Document Type: Conference Paper

References (59)

1. González, J.M., Navarro-Puche, A., Casar, B., Crespo, P. and Andrés, V. (2008) Fast regulation of AP-1 activity through interaction of lamin A/C, ERK1/2, and c-Fos at the nuclear envelope. J. Cell Biol. 183, 653-666
2. Rodríguez, J., Calvo, F., González, J.M., Casar, B., Andrés, V. and Crespo, P. (2010) ERK1/2 MAP kinases promote cell cycle entry by rapid, kinase-independent disruption of retinoblastoma-lamin A complexes. J. Cell Biol. 191, 967-979
3. Broers, J.L., Ramaekers, F.C., Bonne, G., Yaou, R.B. and Hutchison, C.J. (2006) Nuclear lamins: laminopathies and their role in premature ageing. Physiol. Rev. 86, 967-1008 (Pubitemid 44042881)
4. Andrés, V. and González, J.M. (2009) Role of A-type lamins in signaling, transcription, and chromatin organization. J. Cell Biol. 187, 945-957
5. Trigueros-Motos, L., González, J.M., Rivera, J. and Andrés, V. (2011) Hutchinson-Gilford progeria syndrome, cardiovascular disease and oxidative stress. Front. Biosci. (Schol. Ed.) 3, 1285-1297
6. González, J.M., Pla, D., Perez-Sala, D. and Andrés, V. (2011) A-type lamins and Hutchinson-Gilford progeria syndrome: pathogenesis and therapy. Front. Biosci. (Schol. Ed.) 3, 1133-1146
7. Zhang, F.L. and Casey, P.J. (1996) Protein prenylation: molecular mechanisms and functional consequences. Annu. Rev. Biochem. 65, 241-269 (Pubitemid 26250610)
8. Kilic, F., Johnson, D.A. and Sinensky, M. (1999) Subcellular localization and partial purification of prelamin A endoprotease: an enzyme which catalyzes the conversion of farnesylated prelamin A to mature lamin A. FEBS Lett. 450, 61-65 (Pubitemid 29206713)
9. Barrowman, J., Hamblet, C., George, C.M. and Michaelis, S. (2008) Analysis of prelamin A biogenesis reveals the nucleus to be a CaaX processing compartment. Mol. Biol. Cell 19, 5398-5408
10. Goldberg, M.W., Fiserova, J., Huttenlauch, I. and Stick, R. (2008) A new model for nuclear lamina organization. Biochem. Soc. Trans. 36, 1339-1343
11. Dechat, T., Adam, S.A., Taimen, P., Shimi, T. and Goldman, R.D. (2011) Nuclear lamins. Cold Spring Harbor Perspect. Biol. 2, a000547
12. Tapley, E.C., Ly, N. and Starr, D.A. (2011) Multiple mechanisms actively target the SUN protein UNC-84 to the inner nuclear membrane. Mol. Biol. Cell 22, 1739-1752
13. Ostlund, C., Sullivan, T., Stewart, C.L. and Worman, H.J. (2006) Dependence of diffusional mobility of integral inner nuclear membrane proteins on A-type lamins. Biochemistry 45, 1374-1382 (Pubitemid 43214802)
14. Soullam, B. and Worman, H.J. (1993) The amino-terminal domain of the lamin B receptor is a nuclear envelope targeting signal. J. Cell Biol. 120, 1093-1100 (Pubitemid 23064164)
15. Wilson, K.L. and Foisner, R. (2010) Lamin-binding Proteins. Cold Spring Harbor Perspect. Biol. 2, a000554
16. Ostlund, C., Folker, E.S., Choi, J.C., Gomes, E.R., Gundersen, G.G. and Worman, H.J. (2009) Dynamics and molecular interactions of linker of nucleoskeleton and cytoskeleton (LINC) complex proteins. J. Cell Sci. 122, 4099-4108
17. 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
18. Rothman, J.E. (1994) Mechanisms of intracellular protein transport. Nature 372, 55-63
19. Hetzer, M., Meyer, H.H., Walther, T.C., Bilbao-Cortes, D., Warren, G. and Mattaj, I.W. (2001) Distinct AAA-ATPase p97 complexes function in discrete steps of nuclear assembly. Nat. Cell Biol. 3, 1086-1091 (Pubitemid 33130459)
20. Theerthagiri, G., Eisenhardt, N., Schwarz, H. and Antonin, W. (2010) The nucleoporin Nup188 controls passage of membrane proteins across the nuclear pore complex. J. Cell Biol. 189, 1129-1142
21. Turgay, Y., Ungricht, R., Rothballer, A., Kiss, A., Csucs, G., Horvath, P. and Kutay, U. (2010) A classical NLS and the SUN domain contribute to the targeting of SUN2 to the inner nuclear membrane. EMBO J. 29, 2262-2275
22. Zuleger, N., Korfali, N. and Schirmer, E.C. (2008) Inner nuclear membrane protein transport is mediated by multiple mechanisms. Biochem. Soc. Trans. 36, 1373-1377
23. Lusk, C.P., Blobel, G. and King, M.C. (2007) Highway to the inner nuclear membrane: rules for the road. Nat. Rev. Mol. Cell Biol. 8, 414-420 (Pubitemid 46643242)
24. Lu, X., Shi, Y., Lu, Q., Ma, Y., Luo, J., Wang, Q., Ji, J., Jiang, Q. and Zhang, C. (2010) Requirement for lamin B receptor and its regulation by importin β and phosphorylation in nuclear envelope assembly during mitotic exit. J. Biol. Chem. 285, 33281-33293
25. Xu, D., Farmer, A. and Chook, Y.M. (2010) Recognition of nuclear targeting signals by karyopherin-β proteins. Curr. Opin. Struct. Biol. 20, 782-790
26. Saksena, S., Summers, M.D., Burks, J.K., Johnson, A.E. and Braunagel, S.C. (2006) Importin-α-16 is a translocon-associated protein involved in sorting membrane proteins to the nuclear envelope. Nat. Struct. Mol. Biol. 13, 500-508 (Pubitemid 43848904)
27. Braunagel, S.C., Williamson, S.T., Ding, Q., Wu, X. and Summers, M.D. (2007) Early sorting of inner nuclear membrane proteins is conserved. Proc. Natl. Acad. Sci. U.S.A. 104, 9307-9312 (Pubitemid 47185775)
28. Zuleger, N., Kelly, D.A., Richardson, A.C., Kerr, A.R., Goldberg, M.W., Goryachev, A.B. and Schirmer, E.C. (2011) System analysis shows distinct mechanisms and common principles of nuclear envelope protein dynamics. J. Cell Biol. 193, 109-123
29. 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
30. Hennekes, H., Peter, M., Weber, K. and Nigg, E.A. (1993) Phosphorylation on protein kinase C sites inhibits nuclear import of lamin B2. J. Cell Biol. 120, 1293-1304 (Pubitemid 23081678)
31. Leukel, M. and Jost, E. (1995) Two conserved serines in the nuclear localization signal flanking region are involved in the nuclear targeting of human lamin A. Eur. J. Cell Biol. 68, 133-142
32. Broers, J.L. and Ramaekers, F.C. (2004) Dynamics of nuclear lamina assembly and disassembly. Symp. Soc. Exp. Biol. 177-192
33. Dagenais, A., LeMyre, A. and Bibor-Hardy, V. (1990) Differential transport and integration into the nuclear lamina for lamins A, B, and C. Biochem. Cell Biol. 68, 827-831 (Pubitemid 20277160)
34. 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
35. 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 (Pubitemid 351228454)
36. Delbarre, E., Tramier, M., Coppey-Moisan, M., Gaillard, C., Courvalin, J.C. and Buendia, B. (2006) The truncated prelamin A in Hutchinson-Gilford progeria syndrome alters segregation of A-type and B-type lamin homopolymers. Hum. Mol. Genet. 15, 1113-1122
37. 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
38. Vergnes, L., Peterfy, M., Bergo, M.O., Young, S.G. and Reue, K. (2004) Lamin B1 is required for mouse development and nuclear integrity. Proc. Natl. Acad. Sci. U.S.A. 101, 10428-10433 (Pubitemid 38924942)
39. Tang, C.W., Maya-Mendoza, A., Martin, C., Zeng, K., Chen, S., Feret, D., Wilson, S.A. and Jackson, D.A. (2008) The integrity of a lamin-B1-dependent nucleoskeleton is a fundamental determinant of RNA synthesis in human cells. J. Cell Sci. 121, 1014-1024 (Pubitemid 351639420)
40. Guttinger, S., Laurell, E. and Kutay, U. (2009) Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat. Rev. Mol. Cell Biol. 10, 178-191
41. Kutay, U. and Hetzer, M.W. (2008) Reorganization of the nuclear envelope during open mitosis. Curr. Opin. Cell Biol. 20, 669-677
42. Dultz, E., Zanin, E., Wurzenberger, C., Braun, M., Rabut, G., Sironi, L. and Ellenberg, J. (2008) Systematic kinetic analysis of mitotic dis- and reassembly of the nuclear pore in living cells. J. Cell Biol. 180, 857-865 (Pubitemid 351398413)
43. Katsani, K.R., Karess, R.E., Dostatni, N. and Doye, V. (2008) In vivo dynamics of Drosophila nuclear envelope components. Mol. Biol. Cell 19, 3652-3666
44. Beaudouin, J., Gerlich, D., Daigle, N., Eils, R. and Ellenberg, J. (2002) Nuclear envelope breakdown proceeds by microtubule-induced tearing of the lamina. Cell 108, 83-96 (Pubitemid 34137014)
45. Gerace, L. and Blobel, G. (1980) The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell 19, 277-287 (Pubitemid 10154232)
46. Georgatos, S.D., Pyrpasopoulou, A. and Theodoropoulos, P.A. (1997) Nuclear envelope breakdown in mammalian cells involves stepwise lamina disassembly and microtubule-drive deformation of the nuclear membrane. J. Cell Sci. 110, 2129-2140 (Pubitemid 27440436)
47. 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
48. Heald, R. and McKeon, F. (1990) Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 61, 579-589
49. Puhka, M., Vihinen, H., Joensuu, M. and Jokitalo, E. (2007) Endoplasmic reticulum remains continuous and undergoes sheet-to-tubule transformation during cell division in mammalian cells. J. Cell Biol. 179, 895-909 (Pubitemid 350223487)
50. Audhya, A., Desai, A. and Oegema, K. (2007) A role for Rab5 in structuring the endoplasmic reticulum. J. Cell Biol. 178, 43-56 (Pubitemid 47026401)
51. Galy, V., Antonin, W., Jaedicke, A., Sachse, M., Santarella, R., Haselmann, U. and Mattaj, I. (2008) A role for gp210 in mitotic nuclear-envelope breakdown. J. Cell Sci. 121, 317-328 (Pubitemid 351356703)
52. Clarke, P.R. and Zhang, C. (2008) Spatial and temporal coordination of mitosis by Ran GTPase. Nat. Rev. Mol. Cell Biol. 9, 464-477 (Pubitemid 351733403)
53. Sheehan, M.A., Mills, A.D., Sleeman, A.M., Laskey, R.A. and Blow, J.J. (1988) Steps in the assembly of replication-competent nuclei in a cell-free system from Xenopus eggs. J. Cell Biol. 106, 1-12 (Pubitemid 18051387)
54. Anderson, D.J. and Hetzer, M.W. (2008) Reshaping of the endoplasmic reticulum limits the rate for nuclear envelope formation. J. Cell Biol. 182, 911-924
55. Anderson, D.J. and Hetzer, M.W. (2007) Nuclear envelope formation by chromatin-mediated reorganization of the endoplasmic reticulum. Nat. Cell Biol. 9, 1160-1166 (Pubitemid 47500492)
56. Haraguchi, T., Kojidani, T., Koujin, T., Shimi, T., Osakada, H., Mori, C., Yamamoto, A. and Hiraoka, Y. (2008) Live cell imaging and electron microscopy reveal dynamic processes of BAF-directed nuclear envelope assembly. J. Cell Sci. 121, 2540-2554
57. Kuga, T., Nozaki, N., Matsushita, K., Nomura, F. and Tomonaga, T. (2010) Phosphorylation statuses at different residues of lamin B2, B1, and A/C dynamically and independently change throughout the cell cycle. Exp. Cell Res. 316, 2301-2312
58. Dechat, T., Shimi, T., Adam, S.A., Rusinol, A.E., Andres, D.A., Spielmann, H.P., Sinensky, M.S. and Goldman, R.D. (2007) Alterations in mitosis and cell cycle progression caused by a mutant lamin A known to accelerate human aging. Proc. Natl. Acad. Sci. U.S.A. 104, 4955-4960 (Pubitemid 47186158)
59. Moir, R.D., Yoon, M., Khuon, S. and Goldman, R.D. (2000) Nuclear lamins A and B1: different pathways of assembly during nuclear envelope formation in living cells. J. Cell Biol. 151, 1155-1168