Contribution of SUN1 Mutations to the Pathomechanism in Muscular Dystrophies

Human Mutation

Volumn 35, Issue 4, 2014, Pages 452-461

  Li, Ping ^a   Meinke, Peter ^b,c   Huong, Le Thi Thanh ^b,d   Wehnert, Manfred ^b   Noegel, Angelika A ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF GREIFSWALD   (Germany)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d NATIONAL INSTITUTE OF HYGIENE AND EPIDEMIOLOGY   (Viet Nam)

Author keywords

Emerin; Lamin; Laminopathy; LINC complex; Nesprin; Nuclear envelope; SUN1

Indexed keywords

EMERIN; LAMIN A; LAMIN B; LAMIN C; MEMBRANE PROTEIN; MUTANT PROTEIN; NESPRIN N; PROTEIN LAP2; PROTEIN SUN1; PROTEIN SUN2; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; LAMINA-ASSOCIATED POLYPEPTIDE 2; LMNA PROTEIN, HUMAN; MICROTUBULE ASSOCIATED PROTEIN; NUCLEAR PROTEIN; SUN1 PROTEIN, HUMAN; THYMOPOIETIN; TMPO PROTEIN, HUMAN;

ADULT; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CASE REPORT; CELL AGING; CELL CYCLE; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL SIZE; CENTROSOME; CHILD; CONTROLLED STUDY; EMD GENE; EMERY DREIFUSS MUSCULAR DYSTROPHY; FEMALE; FIBROBLAST; GENE; GENE MUTATION; HEAT SHOCK; HEAT STRESS; HETEROZYGOTE; HUMAN; HUMAN CELL; HUMAN TISSUE; LAMINOPATHY; MALE; MUTATIONAL ANALYSIS; NUCLEAR SHAPE; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SCHOOL CHILD; SUN1 GENE; WILD TYPE; CELL NUCLEUS MEMBRANE; GENETICS; METABOLISM; MUTATION; PATHOLOGY;

DNA-BINDING PROTEINS; FEMALE; FIBROBLASTS; HUMANS; LAMIN TYPE A; MALE; MEMBRANE PROTEINS; MICROTUBULE-ASSOCIATED PROTEINS; MUSCULAR DYSTROPHY, EMERY-DREIFUSS; MUTATION; NUCLEAR ENVELOPE; NUCLEAR PROTEINS; THYMOPOIETINS;

EID: 84896110315     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.22504     Document Type: Article

References (38)

1. Benson EK, Lee SW, Aaronson SA. 2010. Role of progerin-induced telomere dysfunction in HGPS premature cellular senescence. J Cell Sci 123:2605-2612.
2. Chancellor TJ, Lee J, Thodeti CK, Lele T. 2010. Actomyosin tension exerted on the nucleus through nesprin-1 connections influences endothelial cell adhesion, migration, and cyclic strain-induced reorientation. Biophys J 99:115-123.
3. Chen CY, Chi YH, Mutalif RA, Starost MF, Myers TG, Anderson SA, Stewart CL, Jeang KT. 2012. Accumulation of the inner nuclear envelope protein Sun1 is pathogenic in progeric and dystrophic laminopathies. Cell 149:565-577.
4. Gotic I, Leschnik M, Kolm U, Markovic M, Haubner BJ, Biadasiewicz K, Metzler B, Stewart CL, Foisner R. 2010. Lamina-associated polypeptide 2alpha loss impairs heart function and stress response in mice. Circ Res 106:346-353.
5. Gueneau L, Bertrand AT, Jais JP, Salih MA, Stojkovic T, Wehnert M, Hoeltzenbein M, Spuler S, Saitoh S, Verschueren A, Tranchant C, Beuvin M, et al. 2009. Mutations of the FHL1 gene cause Emery-Dreifuss muscular dystrophy. Am J Hum Genet 85:338-353.
6. Hale CM, Shrestha AL, Khatau SB, Stewart-Hutchinson PJ, Hernandez L, Stewart CL, Hodzic D, Wirtz D. 2008. Dysfunctional connections between the nucleus and the actin and microtubule networks in laminopathic models. Biophys J 95:5462-5475.
7. Haque F, Mazzeo D, Patel JT, Smallwood DT, Ellis JA, Shanahan CM, 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.
8. Hoeltzenbein M, Karow T, Zeller JA, Warzok R, Wulff K, Zschiesche M, Herrmann FH, Grosse-Heitmeyer W, Wehnert MS. 1999. Severe clinical expression in X-linked Emery-Dreifuss muscular dystrophy. Neuromuscul Disord 9:166-170.
9. Houben F, Willems CH, Declercq IL, Hochstenbach K, Kamps MA, Snoeckx LH, Ramaekers FC, Broers JL. 2009. Disturbed nuclear orientation and cellular migration in A-type lamin deficient cells. Biochim Biophys Acta 1793:312-324.
10. Ho JC, Zhou T, Lai WH, Huang Y, Chan YC, Li X, Wong NL, Li Y, Au KW, Guo D, Xu J, Siu CW, et al. 2011. Generation of induced pluripotent stem cell lines from 3 distinct laminopathies bearing heterogeneous mutations in lamin A/C. Aging (Albany NY) 3:380-390.
11. Khurana T, Khurana B, Noegel AA. 2002. LIM proteins: association with the actin cytoskeleton. Protoplasma 219:1-12.
12. Le Dour C, Schneebeli S, Bakiri F, Darcel F, Jacquemont ML, Maubert MA, Auclair M, Jeziorowska D, Reznik Y, Béréziat V, Capeau J, Lascols O, 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.
13. Lee JS, Hale CM, Panorchan P, Khatau SB, George JP, Tseng Y, Stewart CL, Hodzic D, Wirtz D. 2007. Nuclear lamin A/C deficiency induces defects in cell mechanics, polarization, and migration. Biophys J 93:2542-2552.
14. Lei K, Zhu X, Xu R, Shao C, Xu T, Zhuang Y, Han M. 2012. Inner nuclear envelope proteins SUN1 and SUN2 play a prominent role in the DNA damage response. Curr Biol 22:1609-1615.
15. Liang WC, Mitsuhashi H, Keduka E, Nonaka I, Noguchi S, Nishino I, Hayashi YK. 2011. TMEM43 mutations in Emery-Dreifuss muscular dystrophy-related myopathy. Ann Neurol 69:1005-1013.
16. Liu GH, Barkho BZ, Ruiz S, Diep D, Qu J, Yang SL, Panopoulos AD, Suzuki K, Kurian L, Walsh C, Thompson J, Boue S, et al. 2011. Recapitulation of premature ageing with iPSCs from Hutchinson-Gilford progeria syndrome. Nature 472:221-225.
17. Lu W, Gotzmann J, Sironi L, Jaeger VM, Schneider M, Lüke Y, Uhlén M, Szigyarto CA, Brachner A, Ellenberg J, Foisner R, Noegel AA, et al. 2008. Sun1 forms immobile macromolecular assemblies at the nuclear envelope. Biochim Biophys Acta 1783:2415-2426.
18. Lüke Y, Zaim H, Karakesisoglou I, Jaeger VM, Sellin L, Lu W, Schneider M, Neumann S, Beijer A, Munck M, Padmakumar VC, Gloy J, et al. 2008. Nesprin-2 Giant (NUANCE) maintains nuclear envelope architecture and composition in skin. J Cell Sci 121:1887-1898.
19. Meinke P, Nguyen TD, Wehnert MS. 2011. The LINC complex and human disease. Biochem Soc Trans 39:1693-1697.
20. Padmakumar VC, Abraham S, Braune S, Noegel AA, Tunggal B, Karakesisoglou I, Korenbaum E. 2004. Enaptin, a giant actin-binding protein, is an element of the nuclear membrane and the actin cytoskeleton. Exp Cell Res 295:330-339.
21. Padmakumar VC, Libotte T, Lu W, Zaim H, Abraham S, Noegel AA, Gotzmann J, Foisner R, Karakesisoglou I. 2005. The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope. J Cell Sci 118:3419-3430.
22. Paradisi M, McClintock D, Boguslavsky RL, Pedicelli C, Worman HJ, Djabali K. 2005. Dermal fibroblasts in Hutchinson-Gilford progeria syndrome with the lamin A G608G mutation have dysmorphic nuclei and are hypersensitive to heat stress. BMC Cell Biol 6:27.
23. Pratt CH, Curtain M, Donahue LR, Shopland LS. 2011. Mitotic defects lead to pervasive aneuploidy and accompany loss of RB1 activity in mouse LmnaDhe dermal fibroblasts. PLoS ONE 6:e18065.
24. Rashmi RN, Eckes B, Glöckner G, Groth M, Neumann S, Gloy J, Sellin L, Walz G, Schneider M, Karakesisoglou I, Eichinger L, Noegel AA. 2012. The nuclear envelope protein Nesprin-2 has roles in cell proliferation and differentiation during wound healing. Nucleus 3:172-186.
25. Salpingidou G, Smertenko A, Hausmanowa-Petrucewicz I, Hussey PJ, Hutchison CJ. 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.
26. Scharner J, Brown CA, Bower M, Iannaccone ST, Khatri IA, Escolar D, Gordon E, Felice K, Crowe CA, Grosmann C, Meriggioli MN, Asamoah A, et al. 2011. Novel LMNA mutations in patients with Emery-Dreifuss muscular dystrophy and functional characterization of four LMNA mutations. Hum Mutat 32:152-167.
27. Schneider M, Lu W, Neumann S, Brachner A, Gotzmann J, Noegel AA, Karakesisoglou I. 2011. Molecular mechanisms of centrosome and cytoskeleton anchorage at the nuclear envelope. Cell Mol Life Sci 68:1593-1610.
28. Shan J, Al-Rumaihi K, Rabah D, Al-Bozom I, Kizhakayil D, Farhat K, Al-Said S, Kfoury H, Dsouza SP, Rowe J, Khalak HG, Jafri S, et al. 2013. Genome scan study of prostate cancer in Arabs: identification of three genomic regions with multiple prostate cancer susceptibility loci in Tunisians. J Transl Med 11:121.
29. Simon DN, Wilson KL. 2013. Partners and post-translational modifications of nuclear lamins. Chromosoma 122:13-31.
30. Sosa BA, Rothballer A, Kutay U, Schwartz TU. 2012. LINC complexes form by binding of three KASH peptides to domain interfaces of trimeric SUN proteins. Cell 149:1035-1047.
31. Taranum S, Vaylann E, Meinke P, Abraham S, Yang L, Neumann S, Karakesisoglou I, Wehnert M, Noegel AA. 2012. LINC complex alterations in DMD and EDMD/CMT fibroblasts. Eur J Cell Biol 91, 614-628.
32. Taylor MR, Slavov D, Gajewski A, Vlcek S, Ku L, Fain PR, Carniel E, Di Lenarda A, Sinagra G, Boucek MM, Cavanaugh J, Graw SL, et al. 2005. Thymopoietin (lamina-associated polypeptide 2) gene mutation associated with dilated cardiomyopathy. Hum Mutat 26:566-574.
33. Vigouroux C, Auclair M, Dubosclard E, Pouchelet M, Capeau J, Courvalin JC, Buendia B. 2001. Nuclear envelope disorganization in fibroblasts from lipodystrophic patients with heterozygous R482Q/W mutations in the lamin A/C gene. J Cell Sci 114:4459-4468.
34. Wang W, Shi Z, Jiao S, Chen C, Wang H, Liu G, Wang Q, Zhao Y, Greene MI, Zhou Z. 2012. Structural insights into SUN-KASH complexes across the nuclear envelope. Cell Res 22:1440-1452.
35. Xiong H, Rivero F, Euteneuer U, Mondal S, Mana-Capelli S, Larochelle D, Vogel A, Gassen B, Noegel AA. 2008. Dictyostelium Sun-1 connects the centrosome to chromatin and ensures genome stability. Traffic 9:708-724.
36. Zhang Q, Bethmann C, Worth NF, Davies JD, Wasner C, Feuer A, Ragnauth CD, Yi Q, Mellad JA, Warren DT, Wheeler MA, Ellis JA, 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.
37. Zhang X, Lei K, Yuan X, Wu X, Zhuang Y, Xu T, Xu R, Han M. 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. Zhou Z, Du X, Cai Z, Song X, Zhang H, Mizuno T, Suzuki E, Yee MR, Berezov A, Murali R, Wu SL, Karger BL, et al. 2012. Structure of Sad1-UNC84 homology (SUN) domain defines features of molecular bridge in nuclear envelope. J Biol Chem 287:5317-5326.