Prelamin A-mediated nuclear envelope dynamics in normal and laminopathic cells

Biochemical Society Transactions

Volumn 39, Issue 6, 2011, Pages 1698-1704

  Lattanzi, Giovanna ^a  

^a CNR   (Italy)

Author keywords

Emerin; Emery Dreifuss muscular dystrophy (EDMD); Prelamin A; Progeroid laminopathy; SUN1; SUN2

Indexed keywords

BARRIER TO AUTOINTEGRATION FACTOR; EMERIN; LAMIN A; LAMIN C; LINKER OF NUCLEOSKELETON AND CYTOSKELETON PROTEIN; NUCLEAR PROTEIN; PRELAMIN A; PROTEIN PRECURSOR; SUN1 PROTEIN; SUN2 PROTEIN; UNCLASSIFIED DRUG;

CELL NUCLEUS MEMBRANE; CHROMATIN; CONFERENCE PAPER; DISORDERS OF AMINO ACID AND PROTEIN METABOLISM; EMERY DREIFUSS MUSCULAR DYSTROPHY; HUMAN; HUMAN CELL; HUTCHINSON SYNDROME; MANDIBULOACRAL DYSPLASIA WITH TYPE A LIPODYSTROPHY; MANDIBULOACRAL DYSPLASIA WITH TYPE B LIPODYSTROPHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; RESTRICTIVE DERMOPATHY; WERNER SYNDROME;

ANIMALS; DISEASE; HUMANS; LAMIN TYPE A; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; PROTEIN PRECURSORS;

EUKARYOTA;

EID: 81855169436     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20110657     Document Type: Conference Paper

References (53)

1. Lin, F. and Worman, H.J. (1993) Structural organization of the human gene encoding nuclear lamin A and nuclear lamin C. J. Biol. Chem. 268, 16321-16326 (Pubitemid 23229934)
2. Wydner, K.L., McNeil, J.A., Lin, F., Worman, H.J. and Lawrence, J.B. (1996) Chromosomal assignment of human nuclear envelope protein genes LMNA, LMNB1, and LBR by fluorescence in situ hybridization. Genomics 32, 474-478 (Pubitemid 26094354)
3. Bione, S., Maestrini, E., Rivella, S., Mancini, M., Regis, S., Romeo, G. and Toniolo, D. (1994) Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat. Genet. 8, 323-327 (Pubitemid 24375595)
4. Bonne, G., Di Barletta, M.R., Varnous, S., Becane, H.M., Hammouda, E.H., Merlini, L., Muntoni, F., Greenberg, C.R., Gary, F., Urtizberea, J.A. et al. (1999) Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat. Genet. 21, 285-288 (Pubitemid 29124935)
5. Shackleton, S., Lloyd, D.J., Jackson, S.N., Evans, R., Niermeijer, M.F., Singh, B.M., Schmidt, H., Brabant, G., Kumar, S., Durrington, P.N. et al. (2000) LMNA, encoding lamin A/C, is mutated in partial lipodystrophy. Nat. Genet. 24, 153-156 (Pubitemid 30094715)
6. De Sandre-Giovannoli, A., Chaouch, M., Kozlov, S., Vallat, J.M., Tazir, M., Kassouri, N., Szepetowski, P., Hammadouche, T., Vandenberghe, A., Stewart, C.L. et al. (2002) Homozygous defects in LMNA, encoding lamin A/C nuclear-envelope proteins, cause autosomal recessive axonal neuropathy in human (Charcot-Marie-Tooth disorder type 2) and mouse. Am. J. Hum. Genet. 70, 726-736 (Pubitemid 34177926)
7. Novelli, G., Muchir, A., Sangiuolo, F., Helbling-Leclerc, A., D'Apice, M.R., Massart, C., Capon, F., Sbraccia, P., Federici, M., Lauro, R. et al. (2002) Mandibuloacral dysplasia is caused by a mutation in LMNA-encoding lamin A/C. Am. J. Hum. Genet. 71, 426-431 (Pubitemid 34800259)
8. Agarwal, A.K., Fryns, J.P., Auchus, R.J. and Garg, A. (2003) Zinc metalloproteinase, ZMPSTE24, is mutated in mandibuloacral dysplasia. Hum. Mol. Genet. 12, 1995-2001 (Pubitemid 37038808)
9. Navarro, C.L., De Sandre-Giovannoli, A., Bernard, R., Boccaccio, I., Boyer, A., Genevieve, D., Hadj-Rabia, S., Gaudy-Marqueste, C., Smitt, H.S., Vabres, P. et al. (2004) Lamin A and ZMPSTE24 (FACE-1) defects cause nuclear disorganization and identify restrictive dermopathy as a lethal neonatal laminopathy. Hum. Mol. Genet. 13, 2493-2503 (Pubitemid 39377853)
10. 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 (Pubitemid 40852699)
11. De Sandre-Giovannoli, A., Bernard, R., Cau, P., Navarro, C., Amiel, J., Boccaccio, I., Lyonnet, S., Stewart, C.L., Munnich, A., Le Merrer, M. and Levy, N. (2003) Lamin A truncation in Hutchinson-Gilford progeria. Science 300, 2055 (Pubitemid 36760124)
12. Maraldi, N.M. and Lattanzi, G. (2005) Linkage of lamins to fidelity of gene transcription. Crit. Rev. Eukaryotic Gene Expression 15, 277-294
13. Lattanzi, G., Columbaro, M., Mattioli, E., Cenni, V., Camozzi, D., Wehnert, M., Santi, S., Riccio, M., Del Coco, R., Maraldi, N.M. et al. (2007) Pre-lamin A processing is linked to heterochromatin organization. J. Cell. Biochem. 102, 1149-1159 (Pubitemid 350220036)
14. Zhang, J., Lian, Q., Zhu, G., Zhou, F., Sui, L., Tan, C., Mutalif, R.A., Navasankari, R., Zhang, Y., Tse, H.F. et al. (2011) A human iPSC model of Hutchinson Gilford progeria reveals vascular smooth muscle and mesenchymal stem cell defects. Cell Stem Cell 8, 31-45
15. Moir, R.D., Quinlan, R.A. and Stewart, M. (1990) Expression and characterization of human lamin C. FEBS Lett. 268, 301-305 (Pubitemid 20233890)
16. Cenni, V., Capanni, C., Columbaro, M., Ortolani, M., D'Apice, M.R., Novelli, G., Fini, M., Marmiroli, E., Scarano, N.M., Maraldi, S. et al. (2011) Autophagic degradation of famesylated prelamin A as a therapeutic approach to lamin-linked progeria. Eur. J. Histochem., doi:10.4081/ejh.2011.e36
17. Fong, L.G., Ng, J.K., Lammerding, J., Vickers, T.A., Meta, M., Cote, N., Gavino, B., Qiao, X., Chang, S.Y., Young, S.R. et al. (2006) Prelamin A and lamin A appear to be dispensable in the nuclear lamina. J. Clin. Invest. 116, 743-752 (Pubitemid 43326883)
18. Maraldi, N.M. and Lattanzi, G. (2007) Involvement of prelamin A in laminopathies. Crit. Rev. Eukaryotic Gene Expression 17, 317-334 (Pubitemid 47015559)
19. Mattioli, E., Columbaro, M., Capanni, C., Santi, S., Maraldi, N.M., D'Apice, M.R., Novelli, G., Riccio, M., Squarzoni, S., Foisner, R. and Lattanzi, G. (2008) Drugs affecting prelamin A processing: effects on heterochromatin organization. Exp. Cell Res. 314, 453-462
20. Davies, B.S., Coffinier, C., Yang, S.H., Barnes, R.H., 2nd, Jung, H.J., Young, S.G. and Fong, L.G. (2011) Investigating the purpose of prelamin A processing. Nucleus 2, 4-9
21. 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
22. Barton, R.M. and Worman, H.J. (1999) Prenylated prelamin A interacts with Narf, a novel nuclear protein. J. Biol. Chem. 274, 30008-30018
23. 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 (Pubitemid 34428644)
24. Capanni, C., Mattioli, E., Columbaro, M., Lucarelli, E., Parnaik, V.K., Novelli, G., Wehnert, M., Cenni, V., Maraldi, N.M., Squarzoni, S. and Lattanzi, G. (2005) Altered pre-lamin A processing is a common mechanism leading to lipodystrophy. Hum. Mol. Genet. 14, 1489-1502 (Pubitemid 40823458)
25. Caron, M., Auclair, M., Sterlingot, H., Kornprobst, M. and Capeau, J. (2003) Some HIV protease inhibitors alter lamin A/C maturation and stability, SREBP-1 nuclear localization and adipocyte differentiation. AIDS 17, 2437-2444 (Pubitemid 38393315)
26. Dorner, D., Vlcek, S., Foeger, N., Gajewski, A., Makolm, C., Gotzmann, J., Hutchison, C.J. and Foisner, R. (2006) Lamina-associated polypeptide 2αregulates cell cycle progression and differentiation via the retinoblastoma-E2F pathway. J. Cell Biol. 173, 83-93
27. Capanni, C., Del Coco, R., Squarzoni, S., Columbaro, M., Mattioli, E., Camozzi, D., Rocchi, A., Scotlandi, K., Maraldi, N., Foisner, R. and Lattanzi, G. (2008) Prelamin A is involved in early steps of muscle differentiation. Exp. Cell Res. 314, 3628-3637
28. Capanni, C., Cenni, V., Haraguchi, T., Squarzoni, S., Schüchner, S., Ogris, E., Novelli, G., Maraldi, N.M. and Lattanzi, G. (2010) Lamin A precursor induces barrier-to-autointegration factor nuclear localization. Cell Cycle 9, 2600-2610
29. Lutz, R.J., Trujillo, M.A., Denham, K.S., Wenger, L. and Sinensky, M. (1992) Nucleoplasmic localization of prelamin A: implications for prenylation-dependent lamin A assembly into the nuclear lamina. Proc. Natl. Acad. Sci. U.S.A. 89, 3000-3004
30. 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
31. Gonzalez, J.M., Navarro-Puche, A., Casar, B., Crespo, P. and Andres, 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
32. Caron, M., Auclair, M., Donadille, B., Bereziat, V., Guerci, B., Laville, M., Narbonne, H., Bodemer, C., Lascols, O., Capeau, J. and Vigouroux, C. (2007) Human lipodystrophies linked to mutations in A-type lamins and to HIV protease inhibitor therapy are both associated with prelamin A accumulation, oxidative stress and premature cellular senescence. Cell Death Differ. 14, 1759-1767 (Pubitemid 47423643)
33. Kawai, M. and Rosen, C.J. (2011) PPARγ: a circadian transcription factor in adipogenesis and osteogenesis. Nat. Rev. Endocrinol. 6, 629-636
34. Mattioli, E., Columbaro, M., Capanni, C., Maraldi, N.M., Cenni, V., Scotlandi, K., Marino, M.T., Merlini, L., Squarzoni, S. and Lattanzi, G. (2011) Prelamin A-mediated recruitment of SUN1 to the nuclear envelope directs nuclear positioning in human muscle. Cell Death Differ. 18, 1305-1315
35. Xiong, H., Rivero, F., Euteneuer, U., Mondal, S., Mana-Capelli, S., Larochelle, D., Vogel, A., Gassen, B. and Noegel, A.A. (2008) Dictyostelium Sun-1 connects the centrosome to chromatin and ensures genome stability. Traffic 9, 708-724 (Pubitemid 351494302)
36. 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
37. Capanni, C., Del Coco, R., Mattioli, E., Camozzi, D., Columbaro, M., Schena, E., Merlini, L., Squarzoni, S., Maraldi, N.M. and Lattanzi, G. (2009) Emerin-prelamin A interplay in human fibroblasts. Biol. Cell 101, 541-554
38. Holaska, J.M. and Wilson, K.L. (2007) An emerin "proteome": purification of distinct emerin-containing complexes from HeLa cells suggests molecular basis for diverse roles including gene regulation, mRNA splicing, signaling, mechanosensing, and nuclear architecture. Biochemistry 46, 8897-8908 (Pubitemid 47204453)
39. 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
40. Araujo-Vilar, D., Lattanzi, G., Gonzalez-Mendez, B., Costa-Freitas, A.T., Prieto, D., Columbaro, M., Mattioli, E., Victoria, B., Martinez-Sanchez, N., Ramazanova, A. et al. (2009) Site-dependent differences in both prelamin A and adipogenic genes in subcutaneous adipose tissue of patients with type 2 familial partial lipodystrophy. J. Med. Genet. 46, 40-48
41. Columbaro, M., Capanni, C., Mattioli, E., Novelli, G., Parnaik, V.K., Squarzoni, S., Maraldi, N.M. and Lattanzi, G. (2005) Rescue of heterochromatin organization in Hutchinson-Gilford progeria by drug treatment. Cell. Mol. Life Sci. 62, 2669-2678 (Pubitemid 41721238)
42. 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
43. Columbaro, M., Capanni, C., Mattioli, E., Novelli, G., Parnaik, V.K., Squarzoni, S., Maraldi, N.M. and Lattanzi, G. (2005) Rescue of heterochromatin organization in Hutchinson-Gilford progeria by drug treatment. Cell. Mol. Life Sci. 62, 2669-2678 (Pubitemid 41721238)
44. Columbaro, M., Mattioli, E., Schena, E., Capanni, C., Cenni, V., Levy, N., Navarro, C.L., Del Coco, R., Squarzoni, S., Camozzi, D. et al. (2010) Prelamin A processing and functional effects in restrictive dermopathy. Cell Cycle 9, 4766-4768
45. Caron-Debarle, M., Lagathu, C., Boccara, F., Vigouroux, C. and Capeau, J. (2010) HIV-associated lipodystrophy: from fat injury to premature aging. Trends Mol. Med. 16, 218-229
46. Le Dour, C., Schneebeli, S., Bakiri, F., Darcel, F., Jacquemont, M.L., Maubert, M.A., Auclair, M., Jeziorowska, D., Reznik, Y., Bereziat, V. et al. (2011) A homozygous mutation of prelamin-A preventing its farnesylation and maturation leads to a severe lipodystrophic phenotype: new insights into the pathogenicity of nonfarnesylated prelamin-A. J. Clin. Endocrinol. Metab. 96, E856-E862
47. Marmiroli, S., Bertacchini, J., Beretti, F., Cenni, V., Guida, M., De Pol, A., Maraldi, N.M. and Lattanzi, G. (2009) A-type lamins and signaling: the PI 3-kinase/Akt pathway moves forward. J. Cell. Physiol. 220, 553-561
48. Filesi, I., Gullotta, F., Lattanzi, G., D'Apice, M.R., Capanni, C., Nardone, A.M., Columbaro, M., Scarano, G., Mattioli, E., Sabatelli, P. et al. (2005) Alterations of nuclear envelope and chromatin organization in mandibuloacral dysplasia, a rare form of laminopathy. Physiol. Genomics 23, 150-158 (Pubitemid 44437974)
49. Prufert, K., Vogel, A. and Krohne, G. (2004) The lamin CxxM motif promotes nuclear membrane growth. J. Cell Sci. 117, 6105-6116 (Pubitemid 40123975)
50. Capanni, C., Cenni, V., Mattioli, E., Sabatelli, P., Ognibene, A., Columbaro, M., Parnaik, V.K., Wehnert, M., Maraldi, N.M., Squarzoni, S. and Lattanzi, G. (2003) Failure of lamin A/C to functionally assemble in R482L mutated familial partial lipodystrophy fibroblasts: altered intermolecular interaction with emerin and implications for gene transcription. Exp. Cell Res. 291, 122-134 (Pubitemid 37345152)
51. Lei, K., Zhang, X., Ding, X., Guo, X., Chen, M., Zhu, B., Xu, T., Zhuang, Y., Xu, R. and Han, M. (2009) SUN1 and SUN2 play critical but partially redundant roles in anchoring nuclei in skeletal muscle cells in mice. Proc. Natl. Acad. Sci. U.S.A. 106, 10207-10212
52. Mejat, A., Decostre, V., Li, J., Renou, L., Kesari, A., Hantai, D., Stewart, C.L., Xiao, X., Hoffman, E., Bonne, G. and Misteli, T. (2009) Lamin A/C-mediated neuromuscular junction defects in Emery-Dreifuss muscular dystrophy. J. Cell Biol. 184, 31-44
53. Puente, X.S., Quesada, V., Osorio, F.G., Cabanillas, R., Cadinanos, J., Fraile, J.M., Ordonez, G.R., Puente, D.A., Gutierrez-Fernandez, A., Fanjul-Fernandez, M. et al. (2011) Exome sequencing and functional analysis identifies BANF1 mutation as the cause of a hereditary progeroid syndrome. Am. J. Hum. Genet. 88, 650-656