Interphase phosphorylation of lamin A

Journal of Cell Science

Volumn 127, Issue 12, 2014, Pages 2683-2696

  Kochin, Vitaly ^a,b,c   Shimi, Takeshi ^d   Torvaldson, Elin ^a,b   Adam, Stephen A ^d   Goldman, Anne ^d   Pack, Chan Gi ^e   Melo Cardenas, Johanna ^d   Imanishi, Susumu Y ^a   Goldman, Robert D ^d   Eriksson, John E ^a,b  

^a TURKU CENTRE FOR BIOTECHNOLOGY   (Finland)

^b ÅBO AKADEMI UNIVERSITY   (Finland)

^c SAPPORO MEDICAL UNIVERSITY   (Japan)

^d NORTHWESTERN UNIVERSITY   (United States)

^e RIKEN   (Japan)

Author keywords

Intermediate filament; Lamin A; Phosphorylation; Sequestration; Signaling

Indexed keywords

LAMIN A; BRD2 PROTEIN, HUMAN; LMNA PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE;

AMINO ACID SUBSTITUTION; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; FEMALE; FLUORESCENCE; HELA CELL LINE; HUMAN; HUMAN CELL; INTERPHASE; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; SITE DIRECTED MUTAGENESIS; ACTIVE TRANSPORT; AMINO ACID SEQUENCE; METABOLISM; MOLECULAR GENETICS; NUCLEAR LAMINA; PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN TRANSPORT;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; HELA CELLS; HUMANS; INTERPHASE; LAMIN TYPE A; MOLECULAR SEQUENCE DATA; NUCLEAR LAMINA; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES;

EID: 84902438413     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.141820     Document Type: Article

References (54)

1. Beausoleil, S. A., Jedrychowski, M., Schwartz, D., Elias, J. E., Villén, J., Li, J., Cohn, M. A., Cantley, L. C. and Gygi, S. P. (2004). Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc. Natl. Acad. Sci. USA 101, 12130-12135.
2. Bertacchini, J., Beretti, F., Cenni, V., Guida, M., Gibellini, F., Mediani, L., Marin, O., Maraldi, N. M., de Pol, A., Lattanzi, G. et al. (2013). The protein kinase Akt/PKB regulates both prelamin A degradation and Lmna gene expression. FASEB J. 27, 2145-2155.
3. Broers, J. L., Machiels, B. M., van Eys, G. J., Kuijpers, H. J., Manders, E. M., van Driel, R. and Ramaekers, F. C. (1999). Dynamics of the nuclear lamina as monitored by GFP-tagged A-type lamins. J. Cell Sci. 112, 3463-3475.
4. Burke, B. and Stewart, C. L. (2002). Life at the edge: the nuclear envelope and human disease. Nat. Rev. Mol. Cell Biol. 3, 575-585.
5. Butin-Israeli, V., Adam, S. A., Goldman, A. E. and Goldman, R. D. (2012). Nuclear lamin functions and disease. Trends Genet. 28, 464-471.
6. Capell, B. C. and Collins, F. S. (2006). Human laminopathies: nuclei gone genetically awry. Nat. Rev. Genet. 7, 940-952.
7. Chou, Y. H., Bischoff, J. R., Beach, D. and Goldman, R. D. (1990). Intermediate filament reorganization during mitosis is mediated by p34cdc2 phosphorylation of vimentin. Cell 62, 1063-1071.
8. Dechat, T., Korbei, B., Vaughan, O. A., Vlcek, S., Hutchison, C. J. and Foisner, R. (2000). Lamina-associated polypeptide 2alpha binds intranuclear A-type lamins. J. Cell Sci. 113, 3473-3484.
9. Dechat, T., Pfleghaar, K., Sengupta, K., Shimi, T., Shumaker, D. K., Solimando, L. and Goldman, R. D. (2008). Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev. 22, 832-853.
10. Dessev, G. N., Iovcheva-Dessev, C. and Goldman, R. D. (1990). Lamin dimers. Presence in the nuclear lamina of surf clam oocytes and release during nuclear envelope breakdown. J. Biol. Chem. 265, 12636-12641.
11. Dessev, G., Iovcheva-Dessev, C., Bischoff, J. R., Beach, D. and Goldman, R. (1991). A complex containing p34cdc2 and cyclin B phosphorylates the nuclear lamin and disassembles nuclei of clam oocytes in vitro. J. Cell Biol. 112, 523-533.
12. Dorner, D., Vlcek, S., Foeger, N., Gajewski, A., Makolm, C., Gotzmann, J., Hutchison, C. J. and Foisner, R. (2006). Lamina-associated polypeptide 2alpha regulates cell cycle progression and differentiation via the retinoblastoma-E2F pathway. J. Cell Biol. 173, 83-93.
13. Dreuillet, C., Tillit, J., Kress, M. and Ernoult-Lange, M. (2002). In vivo and in vitro interaction between human transcription factor MOK2 and nuclear lamin A/C. Nucleic Acids Res. 30, 4634-4642.
14. 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.
15. Enoch, T., Peter, M., Nurse, P. and Nigg, E. A. (1991). p34cdc2 acts as a lamin kinase in fission yeast. J. Cell Biol. 112, 797-807.
16. Eriksson, J. E., Brautigan, D. L., Vallee, R., Olmsted, J., Fujiki, H. and Goldman, R. D. (1992). Cytoskeletal integrity in interphase cells requires protein phosphatase activity. Proc. Natl. Acad. Sci. USA 89, 11093-11097.
17. Eriksson, J. E., Toivola, D. M., Sahlgren, C., Mikhailov, A. and Härmälä-Braskén, A. S. (1998). Strategies to assess phosphoprotein phosphatase and protein kinase-mediated regulation of the cytoskeleton. Methods Enzymol. 298, 542-569.
18. Eriksson, M., Brown, W. T., Gordon, L. B., Glynn, M. W., Singer, J., Scott, L., Erdos, M. R., Robbins, C. M., Moses, T. Y., Berglund, P. et al. (2003). Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423, 293-298.
19. Eriksson, J. E., He, T., Trejo-Skalli, A. V., Härmälä-Braskén, A.-S., Hellman, J., Chou, Y.-H. and Goldman, R. D. (2004). Specific in vivo phosphorylation sites determine the assembly dynamics of vimentin intermediate filaments. J. Cell Sci. 117, 919-932.
20. Eriksson, J. E., Dechat, T., Grin, B., Helfand, B., Mendez, M., Pallari, H.-M. and Goldman, R. D. (2009). Introducing intermediate filaments: from discovery to disease. J. Clin. Invest. 119, 1763-1771.
21. Gerace, L. and Blobel, G. (1980). The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell 19, 277-287.
22. Gerace, L., Blum, A. and Blobel, G. (1978). Immunocytochemical localization of the major polypeptides of the nuclear pore complex-lamina fraction. Interphase and mitotic distribution. J. Cell Biol. 79, 546-566.
23. Goldman, R. D., Shumaker, D. K., Erdos, M. R., Eriksson, M., Goldman, A. E., Gordon, L. B., Gruenbaum, Y., Khuon, S., Mendez, M., Varga, R. et al. (2004). Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc. Natl. Acad. Sci. USA 101, 8963-8968.
24. Goss, V. L., Hocevar, B. A., Thompson, L. J., Stratton, C. A., Burns, D. J. and Fields, A. P. (1994). Identification of nuclear beta II protein kinase C as a mitotic lamin kinase. J. Biol. Chem. 269, 19074-19080.
25. Haas, M. and Jost, E. (1993). Functional analysis of phosphorylation sites in human lamin A controlling lamin disassembly, nuclear transport and assembly. Eur. J. Cell Biol. 62, 237-247.
26. Heald, R. and McKeon, F. (1990). Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 61, 579-589.
27. 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.
28. Ho, C. Y., Jaalouk, D. E., Vartiainen, M. K. and Lammerding, J. (2013). Lamin A/C and emerin regulate MKL1-SRF activity by modulating actin dynamics. Nature 497, 507-511.
29. Hocevar, B. A., Burns, D. J. and Fields, A. P. (1993). Identification of protein kinase C (PKC) phosphorylation sites on human lamin B. Potential role of PKC in nuclear lamina structural dynamics. J. Biol. Chem. 268, 7545-7552.
30. Hutchison, C. J. and Worman, H. J. (2004). A-type lamins: guardians of the soma? Nat. Cell Biol. 6, 1062-1067.
31. Imanishi, S. Y., Kochin, V., Ferraris, S. E., de Thonel, A., Pallari, H.-M., Corthals, G. L. and Eriksson, J. E. (2007). Reference-facilitated phosphoproteomics: fast and reliable phosphopeptide validation by microLCESI-Q-TOF MS/MS. Mol. Cell. Proteomics 6, 1380-1391.
32. Kim, J.-E., Tannenbaum, S. R. and White, F. M. (2005). Global phosphoproteome of HT-29 human colon adenocarcinoma cells. J. Proteome Res. 4, 1339-1346.
33. Kochin, V., Imanishi, S. Y. andEriksson, J.E. (2006). Fast track to a phosphoprotein sketch - MALDI-TOF characterization of TLC-based tryptic phosphopeptide maps at femtomolar detection sensitivity. Proteomics 6, 5676-5682.
34. 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.
35. Lloyd, D. J., Trembath, R. C. and Shackleton, S. (2002). A novel interaction between lamin A and SREBP1: implications for partial lipodystrophy and other laminopathies. Hum. Mol. Genet. 11, 769-777.
36. Lüscher, B., Brizuela, L., Beach, D. and Eisenman, R. N. (1991). A role for the p34cdc2 kinase and phosphatases in the regulation of phosphorylation and disassembly of lamin B2 during the cell cycle. EMBO J. 10, 865-875.
37. Mall, M., Walter, T., Gorjánácz, M., Davidson, I. F., Nga Ly-Hartig, T. B., Ellenberg, J. and Mattaj, I. W. (2012). Mitotic lamin disassembly is triggered by lipid-mediated signaling. J. Cell Biol. 198, 981-990.
38. Moir, R. D., Montag-Lowy, M. and Goldman, R. D. (1994). Dynamic properties of nuclear lamins: lamin B is associated with sites of DNA replication. J. Cell Biol. 125 1201-1212.
39. 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.
40. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P. and Mann, M. (2006). Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648.
41. Omary, M. B. (2009). "IF-pathies": a broad spectrum of intermediate filamentassociated diseases. J. Clin. Invest. 119, 1756-1762.
42. Otto, H., Dreger, M., Bengtsson, L. and Hucho, F. (2001). Identification of tyrosine-phosphorylated proteins associated with the nuclear envelope. Eur. J. Biochem. 268, 420-428.
43. Pack, C., Saito, K., Tamura, M. and Kinjo, M. (2006). Microenvironment and effect of energy depletion in the nucleus analyzed by mobility of multiple oligomeric EGFPs. Biophys. J. 91, 3921-3936.
44. Pallari, H.-M. and Eriksson, J. E. (2006). Intermediate filaments as signaling platforms. Sci. STKE 2006, pe53.
45. Pekovic, V., Harborth, J., Broers, J. L. V., Ramaekers, F. C. S., van Engelen, B., Lammens, M., von Zglinicki, T., Foisner, R., Hutchison, C. and Markiewicz, E. (2007). Nucleoplasmic LAP2alpha-lamin A complexes are required to maintain a proliferative state in human fibroblasts. J. Cell Biol. 176, 163-172.
46. Peter, M., Nakagawa, J., Dorée, M., Labbé, 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.
47. Peter, M., Heitlinger, E., Häner, M., Aebi, U. and Nigg, E. A. (1991). Disassembly of in vitro formed lamin head-to-tail polymers by CDC2 kinase. EMBO J. 10, 1535-1544.
48. Schofield, A. V. and Bernard, O. (2013). Rho-associated coiled-coil kinase (ROCK) signaling and disease. Crit. Rev. Biochem. Mol. Biol. 48, 301-316.
49. Shimi, T., Pfleghaar, K., Kojima, S., Pack, C.-G., Solovei, I., Goldman, A. E., Adam, S. A., Shumaker, D. K., Kinjo, M., Cremer, T. et al. (2008). The A- and B-type nuclear lamin networks: microdomains involved in chromatin organization and transcription. Genes Dev. 22, 3409-3421.
50. Shimi, T., Butin-Israeli, V., Adam, S. A., Hamanaka, R. B., Goldman, A. E., Lucas, C. A., Shumaker, D. K., Kosak, S. T., Chandel, N. S. and Goldman, R. D. (2011). The role of nuclear lamin B1 in cell proliferation and senescence. Genes Dev. 25, 2579-2593.
51. Shumaker, D. K., Solimando, L., Sengupta, K., Shimi, T., Adam, S. A., Grunwald, A., Strelkov, S. V., Aebi, U., Cardoso, M. C. and Goldman, R. D. (2008). The highly conserved nuclear lamin Ig-fold binds to PCNA: its role in DNA replication. J. Cell Biol. 181, 269-280.
52. Simon, D. N. and Wilson, K. L. (2013). Partners and post-translational modifications of nuclear lamins. Chromosoma 122, 13-31.
53. Swift, J., Ivanovska, I. L., Buxboim, A., Harada, T., Dingal, P. C. D. P., Pinter, J., Pajerowski, J. D., Spinler, K. R., Shin, J.-W., Tewari, M. et al. (2013). Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 341, 1240104.
54. Ward, G. E. and Kirschner, M. W. (1990). Identification of cell cycle-regulated phosphorylation sites on nuclear lamin C. Cell 61, 561-577.