Functions of the nuclear envelope and lamina in development and disease

Biochemical Society Transactions

Volumn 36, Issue 6, 2008, Pages 1329-1334

  Cohen, Tatiana V ^a   Hernandez, Lidia ^b   Stewart, Colin L ^c  

^a CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

Author keywords

Emery Dreifuss muscular dystrophy (EDMD); Hutchinson Gilford progeria syndrome (HGPS); Lamina; Nuclear envelope

Indexed keywords

CELL NUCLEUS MEMBRANE; CHROMATIN; CONFERENCE PAPER; CONGENITAL MALFORMATION; CYTOSKELETON; DEVELOPMENT; GENETIC DISORDER; HUMAN; INTRACELLULAR TRANSPORT; MACROMOLECULE; NONHUMAN; NUCLEAR LAMINA; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEFECT; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; DISEASE MODEL; EMBRYO DEVELOPMENT; GENERAL ASPECTS OF DISEASE; GENETICS; METABOLISM; PATHOLOGY; REVIEW; SKELETAL MUSCLE;

LAMIN;

ANIMALS; DISEASE; DISEASE MODELS, ANIMAL; EMBRYONIC DEVELOPMENT; HUMANS; LAMINS; MUSCLE, STRIATED; NUCLEAR LAMINA;

EID: 59149084777     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0361329     Document Type: Conference Paper

References (54)

1. Burke, B. and Stewart, C.L. (2006) The laminopathies: the functional architecture of the nucleus and its contribution to disease. Annu. Rev. Genomics Hum. Genet. 7, 369-405
2. Furukawa, K. and Hotta, Y. (1993) cDNA cloning of a germ cell specific lamin B3 from mouse spermatocytes and analysis of its function by ectopic expression in somatic cells. EMBO J. 12, 97-106
3. Goldman, R.D., Gruenbaum, Y., Moir, R.D., Shumaker, D.K. and Spann, T.P. (2002) Nuclear lamins: building blocks of nuclear architecture. Genes Dev. 16, 533-547
4. Heessen, S. and Fornerod, M. (2007) The inner nuclear envelope as a transcription factor resting place. EMBO Rep. 8, 914-919
5. 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
6. 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
7. Worman, H.J. and Bonne, G. (2007) "Laminopathies": a wide spectrum of human diseases. Exp. Cell Res. 313, 2121-2133
8. 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
9. Fatkin, D., MacRae, C., Sasaki, T., Wolff, M.R., Porcu, M., Frenneaux, M., Atherton, J., Vidaillet, Jr, H.J., Spudich, S., De Girolami, U. et al. (1999) Missense mutations in the rod domain of the lamin A/C gene as causes of dilated cardiomyopathy and conduction-system disease. N. Engl. J. Med. 341, 1715-1724
10. Muchir, A., Bonne, G., van der Kooi, A.J., van Meegen, M., Baas, F., Bolhuis, P.A., de Visser, M. and Schwartz, K. (2000) Identification of mutations in the gene encoding lamins A/C in autosomal dominant limb girdle muscular dystrophy with atrioventricular conduction disturbances (LGMD1B). Hum. Mol. Genet. 9, 1453-1459
11. 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
12. Brodsky, G.L., Muntoni, F., Miocic, S., Sinagra, G., Sewry, C. and Mestroni, L. (2000) Lamin A/C gene mutation associated with dilated cardiomyopathy with variable skeletal muscle involvement. Circulation 101, 473-476
13. Muntoni, F., Bonne, G., Goldfarb, L.G., Mercuri, E., Piercy, R.J., Burke, M., Yaou, R.B., Richard, P., Recan, D., Shatunov, A. et al. (2006) Disease severity in dominant Emery Dreifuss is increased by mutations in both emerin and desmin proteins. Brain 129, 1260-1268
14. Taylor, M.R., Slavov, D., Gajewski, A., Vlcek, S., Ku, L., Fain, P.R., Carniel, E., Di Lenarda, A., Sinagra, G., Boucek, M.M. et al. (2005) Thymopoietin (lamina-associated polypeptide 2) gene mutation associated with dilated cardiomyopathy. Hum. Mutat. 26, 566-574
15. Zhang, Q., Bethmann, C., Worth, N.F., Davies, J.D., Wasner, C., Feuer, A., Ragnauth, C.D., Yi, Q., Mellad, J.A., Warren, D.T. et al. (2007) Nesprin-1 and -2 are involved in the pathogenesis of Emery Dreifuss muscular dystrophy and are critical for nuclear envelope integrity. Hum. Mol. Genet. 16, 2816-2833
16. Nikolova, V., Leimena, C., McMahon, A.C., Tan, J.C., Chandar, S., Jogia, D., Kesteven, S.H., Michalicek, J., Otway, R., Verheyen, F. et al. (2004) Defects in nuclear structure and function promote dilated cardiomyopathy in lamin A/C-deficient mice. J. Clin. Invest. 113, 357-369
17. 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
18. Wolf, C.M., Wang, L., Alcalai, R., Pizard, A., Burgon, P.G., Ahmad, F., Sherwood, M., Branco, D.M., Wakimoto, H., Fishman, G.I. et al. (2008) Lamin A/C haploinsufficiency causes dilated cardiomyopathy and apoptosis-triggered cardiac conduction system disease. J. Mol. Cell. Cardiol. 44, 293-303
19. Mounkes, L.C., Kozlov, S.V., Rottman, J.N. and Stewart, C.L. (2005) Expression of an LMNA-N195K variant of A-type lamins results in cardiac conduction defects and death in mice. Hum. Mol. Genet. 14, 2167-2180
20. Gordon, L.B., McCarten, K.M., Giobbie-Hurder, A., Machan, J.T., Campbell, S.E., Berns, S.D. and Kieran, M.W. (2007) Disease progression in Hutchinson-Gilford progeria syndrome: impact on growth and development. Pediatrics 120, 824-833
21. Merideth, M.A., Gordon, L.B., Clauss, S., Sachdev, V., Smith, A.C., Perry, M.B., Brewer, C.C., Zalewski, C., Kim, H.J., Solomon, B. et al. (2008) Phenotype and course of Hutchinson-Gilford progeria syndrome. N. Engl. J. Med. 358, 592-604
22. Gordon, L.B., Harten, I.A., Patti, M.E. and Lichtenstein, A.H. (2005) Reduced adiponectin and HDL cholesterol without elevated C-reactive protein: clues to the biology of premature atherosclerosis in Hutchinson-Gilford progeria syndrome. J. Pediatr. 146, 336-341
23. Stehbens, W.E., Delahunt, B., Shozawa, T. and Gilbert-Barness, E. (2001) Smooth muscle cell depletion and collagen types in progeric arteries. Cardiovasc. Pathol. 10, 133-136
24. Ershler, W.B., Ferrucci, L. and Longo, D.L. (2008) Hutchinson-Gilford progeria syndrome. N. Engl. J. Med. 358, 2409-2410
25. Martin, G.M. (1989) Genetic modulation of the senescent phenotype in Homo sapiens. Genome 31, 390-397
26. 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
27. 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
28. Mounkes, L.C., Kozlov, S., Hernandez, L., Sullivan, T. and Stewart, C.L. (2003) A progeroid syndrome in mice is caused by defects in A-type lamins. Nature 423, 298-301
29. Bridger, J.M. and Kill, I.R. (2004) Aging of Hutchinson-Gilford progeria syndrome fibroblasts is characterised by hyperproliferation and increased apoptosis. Exp. Gerontol. 39, 717-724
30. Csoka, A.B., English, S.B., Simkevich, C.P., Ginzinger, D.G., Butte, A.J., Schatten, G.P., Rothman, F.G. and Sedivy, J.M. (2004) Genome-scale expression profiling of Hutchinson-Gilford progeria syndrome reveals widespread transcriptional misregulation leading to mesodermal/ mesenchymal defects and accelerated atherosclerosis. Aging Cell 3, 235-243
31. Yang, S.H., Bergo, M.O., Toth, J.I., Qiao, X., Hu, Y., Sandoval, S., Meta, M., Bendale, P., Gelb, M.H., Young, S.G. and Fong, L.G. (2005) Blocking protein farnesyltransferase improves nuclear blebbing in mouse .broblasts with a targeted Hutchinson-Gilford progeria syndrome mutation. Proc. Natl. Acad. Sci. U.S.A. 102, 10291-10296
32. Yang, S.H., Meta, M., Qiao, X., Frost, D., Bauch, J., Coffinier, C., Majumdar, S., Bergo, M.O., Young, S.G. and Fong, L.G. (2006) A farnesyltransferase inhibitor improves disease phenotypes in mice with a Hutchinson-Gilford progeria syndrome mutation. J. Clin. Invest. 116, 2115-2121
33. Ostlund, C., Bonne, G., Schwartz, K. and Worman, H.J. (2001) Properties of lamin A mutants found in Emery-Dreifuss muscular dystrophy, cardiomyopathy and Dunnigan-type partial lipodystrophy. J. Cell Sci. 114, 4435-4445
34. Raharjo, W.H., Enarson, P., Sullivan, T., Stewart, C.L. and Burke, B. (2001) Nuclear envelope defects associated with LMNA mutations cause dilated cardiomyopathy and Emery-Dreifuss muscular dystrophy. J. Cell Sci. 114, 4447-4457
35. Lammerding, J., Schulze, P.C., Takahashi, T., Kozlov, S., Sullivan, T., Kamm, R.D., Stewart, C.L. and Lee, R.T. (2004) Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J. Clin. Invest. 113, 370-378
36. 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
37. Lammerding, J., Hsiao, J., Schulze, P.C., Kozlov, S., Stewart, C.L. and Lee, R.T. (2005) Abnormal nuclear shape and impaired mechanotransduction in emerin-deficient cells. J. Cell Biol. 170, 781-791
38. Holaska, J.M., Rais-Bahrami, S. and Wilson, K.L. (2006) Lmo7 is an emerin-binding protein that regulates the transcription of emerin and many other muscle-relevant genes. Hum. Mol. Genet. 15, 3459-3472
39. Holaska, J.M. and Wilson, K.L. (2006) Multiple roles for emerin: implications for Emery-Dreifuss muscular dystrophy. Anat. Rec. A Discov. Mol. Cell Evol. Biol. 288, 676-680
40. 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
41. Lee, J.S., Hale, C.M., Panorchan, P., Khatau, S.B., George, J.P., Iseng, Y., Stewart, C.L., Hodzic, D. and Wirtz, D. (2007) Nuclear lamin A/C deficiency induces defects in cell mechanics, polarization, and migration. Biophys. J. 93, 2542-2552
42. Salpingidou, G., Smertenko, A., Hausmanowa-Petrucewicz, I., Hussey, P.J. and Hutchison, C.J. (2007) A novel role for the nuclear membrane protein emerin in association of the centrosome to the outer nuclear membrane. J. Cell Biol. 178, 897-904
43. Ozawa, R., Hayashi, Y.K., Ogawa, M., Kurokawa, R., Matsumoto, H., Noguchi, S., Nonaka, I. and Nishino, I. (2006) Imerin-lacking mice show minimal motor and cardiac dysfunctions with nuclear-associated vacuoles, Am. J. Pathol. 168, 907-917
44. Takahashi, C., Bronson, R.T., Socolovsky, M., Contreras, B., Lee, K.Y., Jacks, T., Noda, M., Kucherlapati, R. and Ewen, M.E. (2003) Rb and N-ras function together to control differentiation in the mouse. Mol. Cell. Biol. 23, 5256-5268
45. Johnson, B.R., Nitta, R.T., Frock, R.L., Mounkes, L., Barbie, D.A., Stewart, C.L., Hadow, 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
46. 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
47. 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 mustle regeneration. Brain 129, 996-1013
48. Frock, R.L., Kudlow, B.A., Evans, A.M., Jameson, S.A., Hauschka, S.D. and Kennedy, B.K. (2006) Lamin A/C and emerin are critical for skeletal muscle satellite cell differentiation. Genes Dev. 20, 486-500
49. Cao, K., Capell, B.C., Erdos, M.R., Djabali, K. and Collins, F.S. (2007) A lamin A protein isoform overexpressed in Hutchinson-Gilford progeria syndrome interferes with mitosis in progeria and normal cells. Proc. Natl. Acad. Sci. U.S.A. 104, 4949-4954
50. 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. Nail. Acad. Sci. U.S.A. 104, 4955-4960
51. Varga, R., Erksson, M., Erdos, M.R., Olive, M., Harten, I., Kolodgie, F., Capell, B.C., Cheng, J., Faddah, D., Perkins, S. et al. (2006) Progressive vascular smooth muscle cell defects in a mouse model of Hutchinson-Gifford progeria syndrome. Proc. Natl. Acad. Sci. U.S.A. 103, 3250-3255
52. 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. and Collins, F.S. (2004) Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc Natl. Acad. Sci. U.S.A. 101, 8963-8968
53. Verstraeten, V.L., Ji, J.Y., Cummings, K.S., Lee, R.T. and Lammerding, J. (2008) Increased mechanosensitivity and nuclear stiffness in Hutchinson-Gilford progeria cells: effects of farnesyltransferase inhibitors. Aging Cell 7, 383-393
54. Cutler, D.A., Sullivan, T., Marcus-Samuels, B., Stewart, C.L. and Reitman, M.L. (2002) Characterization of adiposity and metabolism in Lmna-deficient mice. Brochem. Biophys. Res. Commun. 291, 522-527