Linker of nucleoskeleton and cytoskeleton complex proteins in cardiac structure, function, and disease

Circulation Research

Volumn 114, Issue 3, 2014, Pages 538-548

  Stroud, Matthew J ^a   Banerjee, Indroneal ^a   Veevers, Jennifer ^a   Chen, Ju ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

cardiac; cardiomyopathies; cell nucleus; myocytes

Indexed keywords

CARDIOMYOPATHIES; CELL NUCLEUS; MYOCYTES, CARDIAC;

ANIMALS; CYTOSKELETON; HEART DISEASES; HUMANS; MYOCYTES, CARDIAC; NUCLEAR MATRIX; PLAKINS;

EID: 84894136024     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.114.301236     Document Type: Review

References (144)

1. Görlich D, Kutay U. Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol. 1999;15:607-660.
2. Brohawn SG, Partridge JR, Whittle JR, Schwartz TU. The nuclear pore complex has entered the atomic age. Structure. 2009;17:1156-1168.
3. Grossman E, Medalia O, Zwerger M. Functional architecture of the nuclear pore complex. Annu Rev Biophys. 2012;41:557-584.
4. Burke B, Stewart CL. The nuclear lamins: flexibility in function. Nat Rev Mol Cell Biol. 2013;14:13-24.
5. Crisp M, Liu Q, Roux K, Rattner JB, Shanahan C, Burke B, Stahl PD, Hodzic D. Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol. 2006;172:41-53.
6. Sosa BA, Kutay U, Schwartz TU. Structural insights into LINC complexes. Curr Opin Struct Biol. 2013;23:285-291.
7. Haque F, Lloyd DJ, Smallwood DT, Dent CL, Shanahan CM, Fry AM, Trembath RC, Shackleton S. SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton. Mol Cell Biol. 2006;26:3738-3751.
8. Padmakumar VC, Libotte T, Lu W, Zaim H, Abraham S, Noegel AA, Gotzmann J, Foisner R, Karakesisoglou I. The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope. J Cell Sci. 2005;118:3419-3430.
9. Sosa BA, Rothballer A, Kutay U, Schwartz TU. LINC complexes form by binding of three KASH peptides to domain interfaces of trimeric SUN proteins. Cell. 2012;149:1035-1047.
10. Starr DA, Fridolfsson HN. Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu Rev Cell Dev Biol. 2010;26:421-444.
11. Starr DA, Han M. Role of ANC-1 in tethering nuclei to the actin cytoskeleton. Science. 2002;298:406-409.
12. Jaalouk DE, Lammerding J. Mechanotransduction gone awry. Nat Rev Mol Cell Biol. 2009;10:63-73.
13. Lombardi ML, Lammerding J. Keeping the LINC: the importance of nucleocytoskeletal coupling in intracellular force transmission and cellular function. Biochem Soc Trans. 2011;39:1729-1734.
14. Mammoto A, Mammoto T, Ingber DE. Mechanosensitive mechanisms in transcriptional regulation. J Cell Sci. 2012;125:3061-3073.
15. Puckelwartz MJ, Depreux FF, McNally EM. Gene expression, chromosome position and lamin A/C mutations. Nucleus. 2011;2:162-167.
16. Wang N, Tytell JD, Ingber DE. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol. 2009;10:75-82.
17. Dellefave L, McNally EM. The genetics of dilated cardiomyopathy. Curr Opin Cardiol. 2010;25:198-204.
18. Méjat A, Misteli T. LINC complexes in health and disease. Nucleus. 2010;1:40-52.
19. Worman HJ, Ostlund C, Wang Y. Diseases of the nuclear envelope. Cold Spring Harb Perspect Biol. 2010;2:a000760.
20. Meinke P, Nguyen TD, Wehnert MS. The LINC complex and human disease. Biochem Soc Trans. 2011;39:1693-1697.
21. Méndez-López I, Worman HJ. Inner nuclear membrane proteins: impact on human disease. Chromosoma. 2012;121:153-167.
22. Zhang Q, Ragnauth C, Greener MJ, Shanahan CM, Roberts RG. The nesprins are giant actin-binding proteins, orthologous to Drosophila melanogaster muscle protein MSP-300. Genomics. 2002;80:473-481.
23. Warren DT, Zhang Q, Weissberg PL, Shanahan CM. Nesprins: intracellular scaffolds that maintain cell architecture and coordinate cell function? Expert Rev Mol Med. 2005;7:1-15.
24. Apel ED, Lewis RM, Grady RM, Sanes JR. Syne-1, a dystrophin-and Klarsicht-related protein associated with synaptic nuclei at the neuromuscular junction. J Biol Chem. 2000;275:31986-31995.
25. Padmakumar VC, Abraham S, Braune S, Noegel AA, Tunggal B, Karakesisoglou I, Korenbaum E. Enaptin, a giant actin-binding protein, is an element of the nuclear membrane and the actin cytoskeleton. Exp Cell Res. 2004;295:330-339.
26. Mislow JM, Kim MS, Davis DB, McNally EM. Myne-1, a spectrin repeat transmembrane protein of the myocyte inner nuclear membrane, interacts with lamin A/C. J Cell Sci. 2002;115:61-70.
27. Shanahan CM, Weissberg PL, Metcalfe JC. Isolation of gene markers of differentiated and proliferating vascular smooth muscle cells. Circ Res. 1993;73:193-204.
28. Zhang Q, Skepper JN, Yang F, Davies JD, Hegyi L, Roberts RG, Weissberg PL, Ellis JA, Shanahan CM. Nesprins: a novel family of spectrin-repeat- containing proteins that localize to the nuclear membrane in multiple tissues. J Cell Sci. 2001;114:4485-4498.
29. Zhen YY, Libotte T, Munck M, Noegel AA, Korenbaum E. NUANCE, a giant protein connecting the nucleus and actin cytoskeleton. J Cell Sci. 2002;115:3207-3222.
30. Simpson JG, Roberts RG. Patterns of evolutionary conservation in the nesprin genes highlight probable functionally important protein domains and isoforms. Biochem Soc Trans. 2008;36:1359-1367.
31. Rajgor D, Mellad JA, Autore F, Zhang Q, Shanahan CM. Multiple novel nesprin-1 and nesprin-2 variants act as versatile tissue-specific intracellular scaffolds. PLoS One. 2012;7:e40098.
32. Zhang Q, Ragnauth CD, Skepper JN, Worth NF, Warren DT, Roberts RG, Weissberg PL, Ellis JA, Shanahan CM. 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. 2005;118:673-687.
33. Rajgor D, Shanahan CM. Nesprins: from the nuclear envelope and beyond. Expert Rev Mol Med. 2013;15:e5.
34. Starr DA, Fischer JA. KASH 'n Karry: the KASH domain family of cargo-specific cytoskeletal adaptor proteins. Bioessays. 2005;27:1136-1146.
35. Mislow JM, Holaska JM, Kim MS, Lee KK, Segura-Totten M, Wilson KL, McNally EM. Nesprin-1alpha self-associates and binds directly to emerin and lamin A in vitro. FEBS Lett. 2002;525:135-140.
36. Zhang Q, Bethmann C, Worth NF, et al. Nesprin-1 and-2 are involved in the pathogenesis of Emery Dreifuss muscular dystrophy and are critical for nuclear envelope integrity. Hum Mol Genet. 2007;16:2816-2833.
37. Puckelwartz MJ, Kessler EJ, Kim G, Dewitt MM, Zhang Y, Earley JU, Depreux FF, Holaska J, Mewborn SK, Pytel P, McNally EM. Nesprin-1 mutations in human and murine cardiomyopathy. J Mol Cell Cardiol. 2010;48:600-608.
38. Wheeler MA, Davies JD, Zhang Q, Emerson LJ, Hunt J, Shanahan CM, Ellis JA. Distinct functional domains in nesprin-1alpha and nesprin-2beta bind directly to emerin and both interactions are disrupted in X-linked Emery-Dreifuss muscular dystrophy. Exp Cell Res. 2007;313:2845-2857.
39. Puckelwartz MJ, Kessler E, Zhang Y, Hodzic D, Randles KN, Morris G, Earley JU, Hadhazy M, Holaska JM, Mewborn SK, Pytel P, McNally EM. Disruption of nesprin-1 produces an Emery Dreifuss muscular dystrophy-like phenotype in mice. Hum Mol Genet. 2009;18:607-620.
40. Stewart-Hutchinson PJ, Hale CM, Wirtz D, Hodzic D. Structural requirements for the assembly of LINC complexes and their function in cellular mechanical stiffness. Exp Cell Res. 2008;314:1892-1905.
41. Malhotra R, Mason PK. Lamin A/C deficiency as a cause of familial dilated cardiomyopathy. Curr Opin Cardiol. 2009;24:203-208.
42. Zhang X, Xu R, Zhu B, Yang X, Ding X, Duan S, Xu T, Zhuang Y, Han M. Syne-1 and Syne-2 play crucial roles in myonuclear anchorage and motor neuron innervation. Development. 2007;134:901-908.
43. Grady RM, Starr DA, Ackerman GL, Sanes JR, Han M. Syne proteins anchor muscle nuclei at the neuromuscular junction. Proc Natl Acad Sci USA. 2005;102:4359-4364.
44. Lüke Y, Zaim H, Karakesisoglou I, Jaeger VM, Sellin L, Lu W, Schneider M, Neumann S, Beijer A, Munck M, Padmakumar VC, Gloy J, Walz G, Noegel AA. Nesprin-2 Giant (NUANCE) maintains nuclear envelope architecture and composition in skin. J Cell Sci. 2008;121:1887-1898.
45. Zhang J, Felder A, Liu Y, Guo LT, Lange S, Dalton ND, Gu Y, Peterson KL, Mizisin AP, Shelton GD, Lieber RL, Chen J. Nesprin 1 is critical for nuclear positioning and anchorage. Hum Mol Genet. 2010;19:329-341.
46. Schirmer EC, Florens L, Guan T, Yates JR III, Gerace L. Nuclear membrane proteins with potential disease links found by subtractive proteomics. Science. 2003;301:1380-1382.
47. Wilhelmsen K, Litjens SH, Kuikman I, Tshimbalanga N, Janssen H, van den Bout I, Raymond K, Sonnenberg A. Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J Cell Biol. 2005;171:799-810.
48. Ketema M, Wilhelmsen K, Kuikman I, Janssen H, Hodzic D, Sonnenberg A. Requirements for the localization of nesprin-3 at the nuclear envelope and its interaction with plectin. J Cell Sci. 2007;120:3384-3394.
49. Ketema M, Kreft M, Secades P, Janssen H, Sonnenberg A. Nesprin-3 connects plectin and vimentin to the nuclear envelope of Sertoli cells but is not required for Sertoli cell function in spermatogenesis. Mol Biol Cell. 2013;24:2454-2466.
50. Postel R, Ketema M, Kuikman I, de Pereda JM, Sonnenberg A. Nesprin-3 augments peripheral nuclear localization of intermediate filaments in zebrafish. J Cell Sci. 2011;124:755-764.
51. Morgan JT, Pfeiffer ER, Thirkill TL, Kumar P, Peng G, Fridolfsson HN, Douglas GC, Starr DA, Barakat AI. Nesprin-3 regulates endothelial cell morphology, perinuclear cytoskeletal architecture, and flow-induced polarization. Mol Biol Cell. 2011;22:4324-4334.
52. Khatau SB, Bloom RJ, Bajpai S, Razafsky D, Zang S, Giri A, Wu PH, Marchand J, Celedon A, Hale CM, Sun SX, Hodzic D, Wirtz D. The distinct roles of the nucleus and nucleus-cytoskeleton connections in three-dimensional cell migration. Sci Rep. 2012;2:488.
53. Roux KJ, Crisp ML, Liu Q, Kim D, Kozlov S, Stewart CL, Burke B. Nesprin 4 is an outer nuclear membrane protein that can induce kinesin-mediated cell polarization. Proc Natl Acad Sci USA. 2009;106:2194-2199.
54. Horn HF, Brownstein Z, Lenz DR, Shivatzki S, Dror AA, Dagan-Rosenfeld O, Friedman LM, Roux KJ, Kozlov S, Jeang KT, Frydman M, Burke B, Stewart CL, Avraham KB. The LINC complex is essential for hearing. J Clin Invest. 2013;123:740-750.
55. Morimoto A, Shibuya H, Zhu X, Kim J, Ishiguro K, Han M, Watanabe Y. A conserved KASH domain protein associates with telomeres, SUN1, and dynactin during mammalian meiosis. J Cell Biol. 2012;198:165-172.
56. Hagan I, Yanagida M. The product of the spindle formation gene sad1+ associates with the fission yeast spindle pole body and is essential for viability. J Cell Biol. 1995;129:1033-1047.
57. Malone CJ, Fixsen WD, Horvitz HR, Han M. UNC-84 localizes to the nuclear envelope and is required for nuclear migration and anchoring during C. elegans development. Development. 1999;126:3171-3181.
58. Xing XW, Li LY, Liu G, Fu JJ, Tan XJ, Lu GX. Identification of a novel gene SRG4 expressed at specific stages of mouse spermatogenesis. Acta Biochim Biophys Sin (Shanghai). 2004;36:351-359.
59. Frohnert C, Schweizer S, Hoyer-Fender S. SPAG4L/SPAG4L-2 are testisspecific SUN domain proteins restricted to the apical nuclear envelope of round spermatids facing the acrosome. Mol Hum Reprod. 2011;17:207-218.
60. Göb E, Schmitt J, Benavente R, Alsheimer M. Mammalian sperm head formation involves different polarization of two novel LINC complexes. PLoS One. 2010;5:e12072.
61. Rothballer A, Schwartz TU, Kutay U. LINCing complex functions at the nuclear envelope: what the molecular architecture of the LINC complex can reveal about its function. Nucleus. 2013;4:29-36.
62. Hodzic DM, Yeater DB, Bengtsson L, Otto H, Stahl PD. Sun2 is a novel mammalian inner nuclear membrane protein. J Biol Chem. 2004;279: 25805-25812.
63. Tapley EC, Ly N, Starr DA. Multiple mechanisms actively target the SUN protein UNC-84 to the inner nuclear membrane. Mol Biol Cell. 2011;22:1739-1752.
64. Zhou Z, Du X, Cai Z, Song X, Zhang H, Mizuno T, Suzuki E, Yee MR, Berezov A, Murali R, Wu SL, Karger BL, Greene MI, Wang Q. Structure of Sad1-UNC84 homology (SUN) domain defines features of molecular bridge in nuclear envelope. J Biol Chem. 2012;287:5317-5326.
65. Wang W, Shi Z, Jiao S, Chen C, Wang H, Liu G, Wang Q, Zhao Y, Greene MI, Zhou Z. Structural insights into SUN-KASH complexes across the nuclear envelope. Cell Res. 2012;22:1440-1452.
66. Göb E, Meyer-Natus E, Benavente R, Alsheimer M. Expression of individual mammalian Sun1 isoforms depends on the cell type. Commun Integr Biol. 2011;4:440-442.
67. Lee KK, Starr D, Cohen M, Liu J, Han M, Wilson KL, Gruenbaum Y. Lamin-dependent localization of UNC-84, a protein required for nuclear migration in Caenorhabditis elegans. Mol Biol Cell. 2002;13:892-901.
68. Hasan S, Güttinger S, Mühlhäusser P, Anderegg F, Bürgler S, Kutay U. Nuclear envelope localization of human UNC84A does not require nuclear lamins. FEBS Lett. 2006;580:1263-1268.
69. Jahn D, Schramm S, Schnölzer M, Heilmann CJ, de Koster CG, Schütz W, Benavente R, Alsheimer M. A truncated lamin A in the Lmna-/-mouse line: implications for the understanding of laminopathies. Nucleus. 2012;3:463-474.
70. Turgay Y, Ungricht R, Rothballer A, Kiss A, Csucs G, Horvath P, Kutay U. A classical NLS and the SUN domain contribute to the targeting of SUN2 to the inner nuclear membrane. EMBO J. 2010;29:2262-2275.
71. Haque F, Mazzeo D, Patel JT, Smallwood DT, Ellis JA, Shanahan CM, Shackleton S. Mammalian SUN protein interaction networks at the inner nuclear membrane and their role in laminopathy disease processes. J Biol Chem. 2010;285:3487-3498.
72. Chen CY, Chi YH, Mutalif RA, Starost MF, Myers TG, Anderson SA, Stewart CL, Jeang KT. Accumulation of the inner nuclear envelope protein Sun1 is pathogenic in progeric and dystrophic laminopathies. Cell. 2012;149:565-577.
73. Lei K, Zhang X, Ding X, Guo X, Chen M, Zhu B, Xu T, Zhuang Y, Xu R, Han M. SUN1 and SUN2 play critical but partially redundant roles in anchoring nuclei in skeletal muscle cells in mice. Proc Natl Acad Sci USA. 2009;106:10207-10212.
74. Bione S, Maestrini E, Rivella S, Mancini M, Regis S, Romeo G, Toniolo D. Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat Genet. 1994;8:323-327.
75. Nagano A, Koga R, Ogawa M, Kurano Y, Kawada J, Okada R, Hayashi YK, Tsukahara T, Arahata K. Emerin deficiency at the nuclear membrane in patients with Emery-Dreifuss muscular dystrophy. Nat Genet. 1996;12:254-259.
76. Manilal S, Nguyen TM, Sewry CA, Morris GE. The Emery-Dreifuss muscular dystrophy protein, emerin, is a nuclear membrane protein. Hum Mol Genet. 1996;5:801-808.
77. Sullivan T, Escalante-Alcalde D, Bhatt H, Anver M, Bhat N, Nagashima K, Stewart CL, Burke B. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol. 1999;147:913-920.
78. Holaska JM, Wilson KL, Mansharamani M. The nuclear envelope, lamins and nuclear assembly. Curr Opin Cell Biol. 2002;14:357-364.
79. Cartegni L, di Barletta MR, Barresi R, Squarzoni S, Sabatelli P, Maraldi N, Mora M, Di Blasi C, Cornelio F, Merlini L, Villa A, Cobianchi F, Toniolo D. Heart-specific localization of emerin: new insights into Emery-Dreifuss muscular dystrophy. Hum Mol Genet. 1997;6:2257-2264.
80. Lee KK, Haraguchi T, Lee RS, Koujin T, Hiraoka Y, Wilson KL. Distinct functional domains in emerin bind lamin A and DNA-bridging protein BAF. J Cell Sci. 2001;114:4567-4573.
81. Berk JM, Tifft KE, Wilson KL. The nuclear envelope LEM-domain protein emerin. Nucleus. 2013;4:298-314.
82. Bione S, Small K, Aksmanovic VM, D'Urso M, Ciccodicola A, Merlini L, Morandi L, Kress W, Yates JR, Warren ST. Identification of new mutations in the Emery-Dreifuss muscular dystrophy gene and evidence for genetic heterogeneity of the disease. Hum Mol Genet. 1995;4:1859-1863.
83. Vohanka S, Vytopil M, Bednarik J, Lukas Z, Kadanka Z, Schildberger J, Ricotti R, Bione S, Toniolo D. A mutation in the X-linked Emery-Dreifuss muscular dystrophy gene in a patient affected with conduction cardiomyopathy. Neuromuscul Disord. 2001;11:411-413.
84. Nigro V, Bruni P, Ciccodicola A, Politano L, Nigro G, Piluso G, Cappa V, Covone AE, Romeo G, D'Urso M. SSCP detection of novel mutations in patients with Emery-Dreifuss muscular dystrophy: definition of a small C-terminal region required for emerin function. Hum Mol Genet. 1995;4:2003-2004.
85. Yamada T, Kobayashi T. A novel emerin mutation in a Japanese patient with Emery-Dreifuss muscular dystrophy. Hum Genet. 1996;97:693-694.
86. Holaska JM. Emerin and the nuclear lamina in muscle and cardiac disease. Circ Res. 2008;103:16-23.
87. Astejada MN, Goto K, Nagano A, Ura S, Noguchi S, Nonaka I, Nishino I, Hayashi YK. Emerinopathy and laminopathy clinical, pathological and molecular features of muscular dystrophy with nuclear envelopathy in Japan. Acta Myol. 2007;26:159-164.
88. Lammerding J, Hsiao J, Schulze PC, Kozlov S, Stewart CL, Lee RT. Abnormal nuclear shape and impaired mechanotransduction in emerin-deficient cells. J Cell Biol. 2005;170:781-791.
89. Ozawa R, Hayashi YK, Ogawa M, Kurokawa R, Matsumoto H, Noguchi S, Nonaka I, Nishino I. Emerin-lacking mice show minimal motor and cardiac dysfunctions with nuclear-associated vacuoles. Am J Pathol. 2006;168:907-917.
90. Rowat AC, Lammerding J, Ipsen JH. Mechanical properties of the cell nucleus and the effect of emerin deficiency. Biophys J. 2006;91:4649-4664.
91. Ho CY, Jaalouk DE, Vartiainen MK, Lammerding J. Lamin A/C and emerin regulate MKL1-SRF activity by modulating actin dynamics. Nature. 2013;497:507-511.
92. Dreger M, Bengtsson L, Schöneberg T, Otto H, Hucho F. Nuclear envelope proteomics: novel integral membrane proteins of the inner nuclear membrane. Proc Natl Acad Sci USA. 2001;98:11943-11948.
93. Bengtsson L, Otto H. LUMA interacts with emerin and influences its distribution at the inner nuclear membrane. J Cell Sci. 2008;121:536-548.
94. Christensen AH, Andersen CB, Tybjaerg-Hansen A, Haunso S, Svendsen JH. Mutation analysis and evaluation of the cardiac localization of TMEM43 in arrhythmogenic right ventricular cardiomyopathy. Clin Genet. 2011;80:256-264.
95. Liang WC, Mitsuhashi H, Keduka E, Nonaka I, Noguchi S, Nishino I, Hayashi YK. TMEM43 mutations in Emery-Dreifuss muscular dystrophy-related myopathy. Ann Neurol. 2011;69:1005-1013.
96. Merner ND, Hodgkinson KA, Haywood AF, Connors S, French VM, Drenckhahn JD, Kupprion C, Ramadanova K, Thierfelder L, McKenna W, Gallagher B, Morris-Larkin L, Bassett AS, Parfrey PS, Young TL. Arrhythmogenic right ventricular cardiomyopathy type 5 is a fully penetrant, lethal arrhythmic disorder caused by a missense mutation in the TMEM43 gene. Am J Hum Genet. 2008;82:809-821.
97. Hodgkinson KA, Connors SP, Merner N, Haywood A, Young TL, McKenna WJ, Gallagher B, Curtis F, Bassett AS, Parfrey PS. The natural history of a genetic subtype of arrhythmogenic right ventricular cardiomyopathy caused by a p.S358L mutation in TMEM43. Clin Genet. 2013;83:321-331.
98. Lemay DG, Hwang DH. Genome-wide identification of peroxisome proliferator response elements using integrated computational genomics. J Lipid Res. 2006;47:1583-1587.
99. Gerace L, Blum A, Blobel G. Immunocytochemical localization of the major polypeptides of the nuclear pore complex-lamina fraction. Interphase and mitotic distribution. J Cell Biol. 1978;79:546-566.
100. Stuurman N, Heins S, Aebi U. Nuclear lamins: their structure, assembly, and interactions. J Struct Biol. 1998;122:42-66.
101. Fisher DZ, Chaudhary N, Blobel G. cDNA sequencing of nuclear lamins A and C reveals primary and secondary structural homology to intermediate filament proteins. Proc Natl Acad Sci USA. 1986;83:6450-6454.
102. McKeon FD, Kirschner MW, Caput D. Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature. 1986;319:463-468.
103. Broers JL, Machiels BM, Kuijpers HJ, Smedts F, van den Kieboom R, Raymond Y, Ramaekers FC. A-and B-type lamins are differentially expressed in normal human tissues. Histochem Cell Biol. 1997;107:505-517.
104. Worman HJ, Courvalin JC. The inner nuclear membrane. J Membr Biol. 2000;177:1-11.
105. Lin F, Worman HJ. Structural organization of the human gene (LMNB1) encoding nuclear lamin B1. Genomics. 1995;27:230-236.
106. Höger TH, Zatloukal K, Waizenegger I, Krohne G. Characterization of a second highly conserved B-type lamin present in cells previously thought to contain only a single B-type lamin. Chromosoma. 1990;100:67-69.
107. Gerace L, Huber MD. Nuclear lamina at the crossroads of the cytoplasm and nucleus. J Struct Biol. 2012;177:24-31.
108. Worman HJ. Nuclear lamins and laminopathies. J Pathol. 2012;226:316-325.
109. Worman HJ, Fong LG, Muchir A, Young SG. Laminopathies and the long strange trip from basic cell biology to therapy. J Clin Invest. 2009;119:1825-1836.
110. Bonne G, Di Barletta MR, Varnous S, Bécane HM, Hammouda EH, Merlini L, Muntoni F, Greenberg CR, Gary F, Urtizberea JA, Duboc D, Fardeau M, Toniolo D, Schwartz K. Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat Genet. 1999;21:285-288.
111. Muchir A, Bonne G, van der Kooi AJ, van Meegen M, Baas F, Bolhuis PA, de Visser M, Schwartz K. 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. 2000;9:1453-1459.
112. Fatkin D, MacRae C, Sasaki T, et al. 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. 1999;341:1715-1724.
113. Renou L, Stora S, Yaou RB, Volk M, Sinkovec M, Demay L, Richard P, Peterlin B, Bonne G. Heart-hand syndrome of Slovenian type: a new kind of laminopathy. J Med Genet. 2008;45:666-671.
114. Quijano-Roy S, Mbieleu B, Bönnemann CG, et al. De novo LMNA mutations cause a new form of congenital muscular dystrophy. Ann Neurol. 2008;64:177-186.
115. Schreiber KH, Kennedy BK. When lamins go bad: nuclear structure and disease. Cell. 2013;152:1365-1375.
116. Sylvius N, Tesson F. Lamin A/C and cardiac diseases. Curr Opin Cardiol. 2006;21:159-165.
117. Prokocimer M, Davidovich M, Nissim-Rafinia M, Wiesel-Motiuk N, Bar DZ, Barkan R, Meshorer E, Gruenbaum Y. Nuclear lamins: key regulators of nuclear structure and activities. J Cell Mol Med. 2009;13:1059-1085.
118. Andrés V, González JM. Role of A-type lamins in signaling, transcription, and chromatin organization. J Cell Biol. 2009;187:945-957.
119. Broers JL, Peeters EA, Kuijpers HJ, Endert J, Bouten CV, Oomens CW, Baaijens FP, Ramaekers FC. Decreased mechanical stiffness in LMNA-/-cells is caused by defective nucleo-cytoskeletal integrity: implications for the development of laminopathies. Hum Mol Genet. 2004;13:2567-2580.
120. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, Solimando L, Goldman RD. Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev. 2008;22:832-853.
121. Folker ES, Ostlund C, Luxton GW, Worman HJ, Gundersen GG. Lamin A variants that cause striated muscle disease are defective in anchoring transmembrane actin-associated nuclear lines for nuclear movement. Proc Natl Acad Sci USA. 2011;108:131-136.
122. Lammerding J, Schulze PC, Takahashi T, Kozlov S, Sullivan T, Kamm RD, Stewart CL, Lee RT. Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J Clin Invest. 2004;113:370-378.
123. Maraldi NM, Capanni C, Cenni V, Fini M, Lattanzi G. Laminopathies and lamin-associated signaling pathways. J Cell Biochem. 2011;112:979-992.
124. Mattout-Drubezki A, Gruenbaum Y. Dynamic interactions of nuclear lamina proteins with chromatin and transcriptional machinery. Cell Mol Life Sci. 2003;60:2053-2063.
125. Wagner N, Krohne G. LEM-Domain proteins: new insights into lamin-interacting proteins. Int Rev Cytol. 2007;261:1-46.
126. Wilson KL, Foisner R. Lamin-binding Proteins. Cold Spring Harb Perspect Biol. 2010;2:a000554.
127. Perrot A, Hussein S, Ruppert V, et al. Identification of mutational hot spots in LMNA encoding lamin A/C in patients with familial dilated cardiomyopathy. Basic Res Cardiol. 2009;104:90-99.
128. Sébillon P, Bouchier C, Bidot LD, Bonne G, Ahamed K, Charron P, Drouin-Garraud V, Millaire A, Desrumeaux G, Benaïche A, Charniot JC, Schwartz K, Villard E, Komajda M. Expanding the phenotype of LMNA mutations in dilated cardiomyopathy and functional consequences of these mutations. J Med Genet. 2003;40:560-567.
129. Mewborn SK, Puckelwartz MJ, Abuisneineh F, Fahrenbach JP, Zhang Y, MacLeod H, Dellefave L, Pytel P, Selig S, Labno CM, Reddy K, Singh H, McNally E. Altered chromosomal positioning, compaction, and gene expression with a lamin A/C gene mutation. PLoS One. 2010;5:e14342.
130. Correa M, Gómez CG. A novel mutation in limb girdle muscular dystrophy. P R Health Sci J. 2007;26:229-232.
131. Bank EM, Gruenbaum Y. The nuclear lamina and heterochromatin: a complex relationship. Biochem Soc Trans. 2011;39:1705-1709.
132. Cremer T, Cremer C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet. 2001;2:292-301.
133. Fraser P, Bickmore W. Nuclear organization of the genome and the potential for gene regulation. Nature. 2007;447:413-417.
134. Verstraeten VL, Broers JL, Ramaekers FC, van Steensel MA. The nuclear envelope, a key structure in cellular integrity and gene expression. Curr Med Chem. 2007;14:1231-1248.
135. Cupesi M, Yoshioka J, Gannon J, Kudinova A, Stewart CL, Lammerding J. Attenuated hypertrophic response to pressure overload in a lamin A/C haploinsufficiency mouse. J Mol Cell Cardiol. 2010;48:1290-1297.
136. Vartiainen MK, Guettler S, Larijani B, Treisman R. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science. 2007;316:1749-1752.
137. Zhang H, Kieckhaefer JE, Cao K. Mouse models of laminopathies. Aging Cell. 2013;12:2-10.
138. Arimura T, Helbling-Leclerc A, Massart C, Varnous S, Niel F, Lacène E, Fromes Y, Toussaint M, Mura AM, Keller DI, Amthor H, Isnard R, Malissen M, Schwartz K, Bonne G. Mouse model carrying H222P-Lmna mutation develops muscular dystrophy and dilated cardiomyopathy similar to human striated muscle laminopathies. Hum Mol Genet. 2005;14:155-169.
139. Nikolova V, Leimena C, McMahon AC, Tan JC, Chandar S, Jogia D, Kesteven SH, Michalicek J, Otway R, Verheyen F, Rainer S, Stewart CL, Martin D, Feneley MP, Fatkin D. Defects in nuclear structure and function promote dilated cardiomyopathy in lamin A/C-deficient mice. J Clin Invest. 2004;113:357-369.
140. Kubben N, Voncken JW, Konings G, van Weeghel M, van den Hoogenhof MM, Gijbels M, van Erk A, Schoonderwoerd K, van den Bosch B, Dahlmans V, Calis C, Houten SM, Misteli T, Pinto YM. Post-natal myogenic and adipogenic developmental: defects and metabolic impairment upon loss of A-type lamins. Nucleus. 2011;2:195-207.
141. van Engelen BG, Muchir A, Hutchison CJ, van der Kooi AJ, Bonne G, Lammens M. The lethal phenotype of a homozygous nonsense mutation in the lamin A/C gene. Neurology. 2005;64:374-376.
142. Vergnes L, Péterfy M, Bergo MO, Young SG, Reue K. Lamin B1 is required for mouse development and nuclear integrity. Proc Natl Acad Sci USA. 2004;101:10428-10433.
143. Padiath QS, Saigoh K, Schiffmann R, Asahara H, Yamada T, Koeppen A, Hogan K, Ptácek LJ, Fu YH. Lamin B1 duplications cause autosomal dominant leukodystrophy. Nat Genet. 2006;38:1114-1123.
144. Coffinier C, Chang SY, Nobumori C, Tu Y, Farber EA, Toth JI, Fong LG, Young SG. Abnormal development of the cerebral cortex and cerebellum in the setting of lamin B2 deficiency. Proc Natl Acad Sci USA. 2010;107:5076-5081.