Lamin A variants that cause striated muscle disease are defective in anchoring transmembrane actin-associated nuclear lines for nuclear movement

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 1, 2011, Pages 131-136

  Folker, Eric S ^a   Östlund, Cecilia ^a,b   Luxton, G W Gant ^a   Worman, Howard J ^a,b   Gundersen, Gregg G ^a  

^a NewYork Presbyterian Hospital   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Linker of nucleoskeleton and cytoskeleton complex; Muscular dystrophy; Nesprin SUN

Indexed keywords

ACTIN; LAMIN A;

ADIPOSE TISSUE; ARTICLE; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL STRAIN 3T3; CENTROSOME; CYTOSKELETON; GENE; GENE DELETION; GENE MUTATION; HUMAN; HUMAN CELL; LMNA GENE; MUSCLE DISEASE; NULL ALLELE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN VARIANT; SKELETAL MUSCLE;

ACTINS; ANIMALS; BIOLOGICAL TRANSPORT; BLOTTING, WESTERN; CELL NUCLEUS; CENTROSOME; FLUORESCENT ANTIBODY TECHNIQUE; LAMIN TYPE A; MEMBRANE PROTEINS; MICE; MUSCLE, STRIATED; MUSCULAR DISEASES; MUTATION; NERVE TISSUE PROTEINS; NIH 3T3 CELLS; NUCLEAR PROTEINS; RNA, SMALL INTERFERING; TELOMERE-BINDING PROTEINS;

MAMMALIA;

EID: 78651103909     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1000824108     Document Type: Article

References (40)

1. Bonne G, et al. (1999) Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat Genet 21:285-288.
2. Shackleton S, et al. (2000) LMNA, encoding lamin A/C, is mutated in partial lipodystrophy. Nat Genet 24:153-156.
3. De Sandre-Giovannoli A, 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.
4. De Sandre-Giovannoli A, et al. (2003) Lamin a truncation in Hutchinson-Gilford progeria. Science 300:2055.
5. Eriksson M, et al. (2003) Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423:293-298.
6. Broers JL, et al. (2004) Decreased mechanical stiffness in LMNA-/- cells is caused by defective nucleo-cytoskeletal integrity: Implications for the development of laminopathies. Hum Mol Genet 13:2567-2580.
7. Lammerding J, et al. (2004) Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J Clin Invest 113:370-378.
8. Bakay M, et al. (2006) Nuclear envelope dystrophies show a transcriptional fingerprint suggesting disruption of Rb-MyoD pathways in muscle regeneration. Brain 129:996-1013.
9. Crisp M, et al. (2006) Coupling of the nucleus and cytoplasm: Role of the LINC complex. J Cell Biol 172:41-53.
10. Worman HJ, Gundersen GG (2006) Here come the SUNs: A nucleocytoskeletal missing link. Trends Cell Biol 16:67-69.
11. Starr DA, Han M (2003) ANChors away: An actin based mechanism of nuclear positioning. J Cell Sci 116:211-216.
12. Starr DA (2009) A nuclear-envelope bridge positions nuclei and moves chromosomes. J Cell Sci 122:577-586.
13. Luxton GW, Gomes ER, Folker ES, Vintinner E, Gundersen GG (2010) Linear arrays of nuclear envelope proteins harness retrograde actin flow for nuclear movement. Science 329:956-959.
14. Patterson K, et al. (2004) The functions of Klarsicht and nuclear lamin in developmentally regulated nuclear migrations of photoreceptor cells in the Drosophila eye. Mol Biol Cell 15:600-610.
15. Guillemin K, Williams T, Krasnow MA (2001) A nuclear lamin is required for cytoplasmic organization and egg polarity in Drosophila. Nat Cell Biol 3:848-851.
16. Lee KK, et al. (2002) Lamin-dependent localization of UNC-84, a protein required for nuclear migration in Caenorhabditis elegans. Mol Biol Cell 13:892-901.
17. Hale CM, et al. (2008) Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models. Biophys J 95:5462-5475.
18. Lee JS, et al. (2007) Nuclear lamin A/C deficiency induces defects in cell mechanics, polarization, and migration. Biophys J 93:2542-2552.
19. Haque F, et al. (2006) SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton. Mol Cell Biol 26:3738-3751.
20. Gomes ER, Jani S, Gundersen GG (2005) Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 121:451-463.
21. Palazzo AF, et al. (2001) Cdc42, dynein, and dynactin regulate MTOC reorientation independent of Rho-regulated microtubule stabilization. Curr Biol 11:1536-1541.
22. Schmoranzer J, et al. (2009) Par3 and dynein associate to regulate local microtubule dynamics and centrosome orientation during migration. Curr Biol 19:1065-1074.
23. Östlund C, Bonne G, Schwartz K, Worman HJ (2001) Properties of lamin A mutants found in Emery-Dreifuss muscular dystrophy, cardiomyopathy and Dunnigan-type partial lipodystrophy. J Cell Sci 114:4435-4445.
24. Houben F, et al. (2009) Disturbed nuclear orientation and cellular migration in A-type lamin deficient cells. Biochim Biophys Acta 1793:312-324.
25. Muchir A, Shan J, Bonne G, Lehnart SE, Worman HJ (2009) Inhibition of extracellular signal-regulated kinase signaling to prevent cardiomyopathy caused by mutation in the gene encoding A-type lamins. Hum Mol Genet 18:241-247.
26. Sullivan T, et al. (1999) Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 147:913-920.
27. Ezratty EJ, Bertaux C, Marcantonio EE, Gundersen GG (2009) Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J Cell Biol 187:733-747.
28. Muchir A, et al. (2004) Nuclear envelope alterations in fibroblasts from patients with muscular dystrophy, cardiomyopathy, and partial lipodystrophy carrying lamin A/C gene mutations. Muscle Nerve 30:444-450.
29. Riedl J, et al. (2008) Lifeact: A versatile marker to visualize F-actin. Nat Methods 5:605-607.
30. Hasan S, et al. (2006) Nuclear envelope localization of human UNC84A does not require nuclear lamins. FEBS Lett 580:1263-1268.
31. Zhang Q, et al. (2005) Nesprin-2 is a multi-isomeric protein that binds lamin and emerin at the nuclear envelope and forms a subcellular network in skeletal muscle. J Cell Sci 118:673-687.
32. Ostlund C, Sullivan T, Stewart CL, Worman HJ (2006) Dependence of diffusional mobility of integral inner nuclear membrane proteins on A-type lamins. Biochemistry 45:1374-1382.
33. Östlund C, et al. (2009) Dynamics and molecular interactions of linker of nucleoskeleton and cytoskeleton (LINC) complex proteins. J Cell Sci 122:4099-4108.
34. Libotte T, et al. (2005) Lamin A/C-dependent localization of Nesprin-2, a giant scaffolder at the nuclear envelope. Mol Biol Cell 16:3411-3424.
35. King MC, Drivas TG, Blobel G (2008) A network of nuclear envelope membrane proteins linking centromeres to microtubules. Cell 134:427-438.
36. Schenk J, Wilsch-Bräuninger M, Calegari F, Huttner WB (2009) Myosin II is required for interkinetic nuclear migration of neural progenitors. Proc Natl Acad Sci USA 106:16487-16492.
37. Zhang X, et al. (2009) SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 64:173-187.
38. Zhang Q, 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.
39. Cook TA, Nagasaki T, Gundersen GG (1998) Rho guanosine triphosphatase mediates the selective stabilization of microtubules induced by lysophosphatidic acid. J Cell Biol 141:175-185.
40. Gomes ER, Gundersen GG (2006) Real-time centrosome reorientation during fibroblast migration. Methods Enzymol 406:579-592.