Structural alterations of lamin A protein in dilated cardiomyopathy

Biochemistry

Volumn 52, Issue 24, 2013, Pages 4229-4241

  Bhattacharjee, Pritha ^a   Banerjee, Avinanda ^a   Banerjee, Amrita ^a   Dasgupta, Dipak ^a   Sengupta, Kaushik ^a  

^a SAHA INSTITUTE OF NUCLEAR PHYSICS   (India)

Author keywords

[No Author keywords available]

Indexed keywords

DILATED CARDIOMYOPATHY; HELICAL COILED-COIL; INNER NUCLEAR MEMBRANES; INTERMEDIATE FILAMENTS; MYOCARDIAL INFARCTION; SECONDARY AND TERTIARY STRUCTURES; SELF-ASSOCIATION BEHAVIOR; STRUCTURAL ALTERATIONS;

ASSOCIATION REACTIONS; CARDIOLOGY; CELL MEMBRANES; GENES;

PROTEINS;

LAMIN A;

ARTICLE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; ENERGY TRANSFER; ENTHALPY; HEART ARRHYTHMIA; HEART INFARCTION; HUMAN; HUMAN CELL; LAMINOPATHY; MUTANT; MUTATION; POINT MUTATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; WILD TYPE;

CARDIOMYOPATHY, DILATED; CELL NUCLEUS; DIASTOLE; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LAMIN TYPE A; LAMINS; MICROSCOPY, FLUORESCENCE; MUTAGENESIS, SITE-DIRECTED; MUTATION; NUCLEAR ENVELOPE; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SYSTOLE;

METAZOA;

EID: 84879221522     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400337t     Document Type: Article

References (68)

1. Cohen, M., Lee, K. K., Wilson, K. L., and Gruenbaum, Y. (2001) Transcriptional repression, apoptosis, human disease and the functional evolution of the nuclear lamina Trends Biochem. Sci. 26, 41-47
2. Melcer, S., Gruenbaum, Y., and Krohne, G. (2007) Invertebrate lamins Exp. Cell Res. 313, 2157-2166
3. 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
4. Machiels, B. M., Zorenc, A. H., Endert, J. M., Kuijpers, H. J., van Eys, G. J., Ramaekers, F. C., and Broers, J. L. (1996) An alternative splicing product of the lamin A/C gene lacks exon 10 J. Biol. Chem. 271, 9249-9253
5. Furukawa, K., Inagaki, H., and Hotta, Y. (1994) Identification and cloning of an mRNA coding for a germ cell-specific A-type lamin in mice Exp. Cell Res. 212, 426-430
6. Peter, M., Kitten, G., Lehner, C., Vorburger, K., Bailer, S., Maridor, G., and Nigg, E. (1989) Cloning and sequencing of cDNA clones encoding chicken lamins A and B1 and comparison of the primary structures of vertebrate A- and B-type lamins J. Mol. Biol. 208, 393
7. Rober, R., 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
8. 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
9. Constantinescu, D., Gray, H. L., Sammak, P. J., Schatten, G. P., and Csoka, A. B. (2006) Lamin A/C expression is a marker of mouse and human embryonic stem cell differentiation Stem Cells 24, 177-185
10. Eckersley-Maslin, M. A., Bergmann, J. H., Lazar, Z., and Spector, D. L. (2013) Lamin A/C is Expressed in Pluripotent Mouse Embryonic Stem Cells Nucleus 4, 53-60
11. Parry, D., Conway, J. F., and Steinert, P. M. (1986) Structural studies on lamin. Similarities and differences between lamin and intermediate-filament proteins Biochem. J. 238, 305
12. Krimm, I., Östlund, C., Gilquin, B., Couprie, J., Hossenlopp, P., Mornon, J. P., Bonne, G., Courvalin, J. C., Worman, H. J., and Zinn-Justin, S. (2002) The Ig-like structure of the C-terminal domain of lamin A/C, mutated in muscular dystrophies, cardiomyopathy, and partial lipodystrophy Structure 10, 811-823
13. Dhe-Paganon, S., Werner, E. D., Chi, Y. I., and Shoelson, S. E. (2002) Structure of the globular tail of nuclear lamin J. Biol. Chem. 277, 17381-17384
14. Strelkov, S. V., Schumacher, J., Burkhard, P., Aebi, U., and Herrmann, H. (2004) Crystal structure of the human lamin A coil 2B dimer: Implications for the head-to-tail association of nuclear lamins J. Mol. Biol. 343, 1067-1080
15. Heitlinger, E., Peter, M., Häner, M., Lustig, A., Aebi, U., and Nigg, E. (1991) Expression of chicken lamin B2 in Escherichia coli: Characterization of its structure, assembly, and molecular interactions J. Cell Biol. 113, 485-495
16. Stuurman, N., Sasse, B., and Fisher, P. A. (1996) Intermediate Filament Protein Polymerization: Molecular Analysis of Drosophila Nuclear Lamin Head-to-Tail Binding J. Struct. Biol. 117, 1-15
17. Ben-Harush, K., Wiesel, N., Frenkiel-Krispin, D., Moeller, D., Soreq, E., Aebi, U., Herrmann, H., Gruenbaum, Y., and Medalia, O. (2009) The Supramolecular Organization of the C. elegans Nuclear Lamin Filament J. Mol. Biol. 386, 1392-1402
18. Zackroff, R. V. and Goldman, R. D. (1979) In vitro assembly of intermediate filaments from baby hamster kidney (BHK-21) cells Proc. Natl. Acad. Sci. U.S.A. 76, 6226-6230
19. 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., Duboc, D., Fardeau, M., Toniolo, D., and Schwartz, K. (1999) Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy Nat. Genet. 21, 285-288
20. Fatkin, D., MacRae, C., Sasaki, T., Wolff, M. R., Porcu, M., Frenneaux, M., Atherton, J., Vidaillet, H. J., Jr., Spudich, S., De Girolami, U., Seidman, J. G., Seidman, C., Muntoni, F., Muehle, G., Johnson, W., and McDonough, B. (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
21. Broers, J., Ramaekers, F., Bonne, G., Yaou, R. B., and Hutchison, C. (2006) Nuclear lamins: Laminopathies and their role in premature ageing Physiol. Rev. 86, 967-1008
22. Kudlow, B. A., Kennedy, B. K., and Monnat, R. J., Jr. (2007) Werner and Hutchinson-Gilford progeria syndromes: Mechanistic basis of human progeroid diseases Nat. Rev. Mol. Cell Biol. 8, 394-404
23. Worman, H. J. and Bonne, G. (2007) "Laminopathies": A wide spectrum of human diseases Exp. Cell Res. 313, 2121-2133
24. Richardson, P., McKenna, W., Bristow, M., Maisch, B., Mautner, B., O'Connell, J., Olsen, E., Thiene, G., Goodwin, J., Gyarfas, I., Martin, I., and Nordet, P. (1996) Report of the 1995 World Health Organization/International Society and Federation of Cardiology Task Force on the Definition and Classification of cardiomyopathies Circulation 93, 841-842
25. Boffa, G. M., Thiene, G., Nava, A., and Dalla Volta, S. (1991) Cardiomyopathy: A necessary revision of the WHO classification Int. J. Cardiol. 30, 1-7
26. Arbustini, E., Pilotto, A., Repetto, A., Grasso, M., Negri, A., Diegoli, M., Campana, C., Scelsi, L., Baldini, E., Gavazzi, A., and Tavazzi, L. (2002) Autosomal dominant dilated cardiomyopathy with atrioventricular block: A lamin A/C defect-related disease J. Am. Coll. Cardiol. 39, 981-990
27. Hermida-Prieto, M., Monserrat, L., Castro-Beiras, A., Laredo, R., Soler, R., Peteiro, J., Rodriguez, E., Bouzas, B., Alvarez, N., Muniz, J., and Crespo-Leiro, M. (2004) Familial dilated cardiomyopathy and isolated left ventricular noncompaction associated with lamin A/C gene mutations Am. J. Cardiol. 94, 50-54
28. Pethig, K., Genschel, J., Peters, T., Wilhelmi, M., Flemming, P., Lochs, H., Haverich, A., and Schmidt, H. H. (2005) LMNA mutations in cardiac transplant recipients Cardiology 103, 57-62
29. Sylvius, N., Bilinska, Z. T., Veinot, J. P., Fidzianska, A., Bolongo, P. M., Poon, S., McKeown, P., Davies, R. A., Chan, K. L., Tang, A. S., Dyack, S., Grzybowski, J., Ruzyllo, W., McBride, H., and Tesson, F. (2005) In vivo and in vitro examination of the functional significances of novel lamin gene mutations in heart failure patients J. Med. Genet. 42, 639-647
30. Cowan, J., Li, D., Gonzalez-Quintana, J., Morales, A., and Hershberger, R. E. (2010) Morphological analysis of 13 LMNA variants identified in a cohort of 324 unrelated patients with idiopathic or familial dilated cardiomyopathy Circ.: Cardiovasc. Genet. 3, 6-14
31. Song, K., Dube, M. P., Lim, J., Hwang, I., Lee, I., and Kim, J. J. (2007) Lamin A/C mutations associated with familial and sporadic cases of dilated cardiomyopathy in Koreans Exp. Mol. Med. 39, 114-120
32. Arbustini, E., Pilotto, A., Grasso, M., Marziliano, N., Serio, A., Gambarin, F., Pasotti, M., Serafini, E., Cassini, P., and Digiorgio, B. (2009) Novel human pathological mutations. Gene symbol: LMNA. Disease: cardiomyopathy, dilated with conduction defects Hum. Genet. 125, 350
33. Vigouroux, C., Auclair, M., Dubosclard, E., Pouchelet, M., Capeau, J., Courvalin, J. C., and 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. 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. 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
36. Moir, R. D., Donaldson, A. D., and Stewart, M. (1991) Expression in Escherichia coli of human lamins A and C: Influence of head and tail domains on assembly properties and paracrystal formation J. Cell Sci. 99 (Part 2) 363-372
37. Slavik, J. (1982) Anilinonaphthalene sulfonate as a probe of membrane composition and function Biochim. Biophys. Acta 694, 1-25
38. Frisken, B. J. (2001) Revisiting the method of cumulants for the analysis of dynamic light-scattering data Appl. Opt. 40, 4087-4091
39. Spann, T. P., Moir, R. D., Goldman, A. E., Stick, R., and Goldman, R. D. (1997) Disruption of nuclear lamin organization alters the distribution of replication factors and inhibits DNA synthesis J. Cell Biol. 136, 1201-1212
40. Bridger, J. M., Kill, I. R., O'Farrell, M., and Hutchison, C. J. (1993) Internal lamin structures within G1 nuclei of human dermal fibroblasts J. Cell Sci. 104 (Part 2) 297-306
41. Machiels, B. M., Broers, J. L., Raymond, Y., de Ley, L., Kuijpers, H. J., Caberg, N. E., and Ramaekers, F. C. (1995) Abnormal A-type lamin organization in a human lung carcinoma cell line Eur. J. Cell Biol. 67, 328-335
42. Jagatheesan, G., Thanumalayan, S., Muralikrishna, B., Rangaraj, N., Karande, A. A., and Parnaik, V. K. (1999) Colocalization of intranuclear lamin foci with RNA splicing factors J. Cell Sci. 112 (Part 24) 4651-4661
43. Broers, J. L., Kuijpers, H. J., Ostlund, C., Worman, H. J., Endert, J., and Ramaekers, F. C. (2005) Both lamin A and lamin C mutations cause lamina instability as well as loss of internal nuclear lamin organization Exp. Cell Res. 304, 582-592
44. Sylvius, N., Hathaway, A., Boudreau, E., Gupta, P., Labib, S., Bolongo, P. M., Rippstein, P., McBride, H., Bilinska, Z. T., and Tesson, F. (2008) Specific contribution of lamin A and lamin C in the development of laminopathies Exp. Cell Res. 314, 2362-2375
45. Mendez, M. G., Kojima, S., and Goldman, R. D. (2010) Vimentin induces changes in cell shape, motility, and adhesion during the epithelial to mesenchymal transition FASEB J. 24, 1838-1851
46. Shumaker, D. K., Solimando, L., Sengupta, K., Shimi, T., Adam, S. A., Grunwald, A., Strelkov, S. V., Aebi, U., Cardoso, M. C., and Goldman, R. D. (2008) The highly conserved nuclear lamin Ig-fold binds to PCNA: Its role in DNA replication J. Cell Biol. 181, 269-280
47. Aebi, U., Cohn, J., Buhle, L., and Gerace, L. (1986) The nuclear lamina is a meshwork of intermediate-type filaments Nature 323, 560-564
48. Takashi, R., Tonomura, Y., and Morales, M. F. (1977) 4,4′-Bis(1- anilinonaphthalene 8-sulfonate) (bis-ANS): A new probe of the active site of myosin Proc. Natl. Acad. Sci. U.S.A. 74, 2334-2338
49. Lau, S., Taneja, A., and Hodges, R. (1984) Synthesis of a model protein of defined secondary and quaternary structure. Effect of chain length on the stabilization and formation of two-stranded α-helical coiled-coils J. Biol. Chem. 259, 13253-13261
50. Whitmore, L. and Wallace, B. (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data Nucleic Acids Res. 32, W668-W673
51. Whitmore, L. and Wallace, B. A. (2007) Protein secondary structure analyses from circular dichroism spectroscopy: Methods and reference databases Biopolymers 89, 392-400
52. Andrade, M., Chacon, P., Merelo, J., and Moran, F. (1993) Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network Protein Eng. 6, 383-390
53. Unneberg, P., Merelo, J. J., Chacon, P., and Moran, F. (2001) SOMCD: Method for evaluating protein secondary structure from UV circular dichroism spectra Proteins 42, 460-470
54. Chen, Y. H., Yang, J. T., and Martinez, H. M. (1972) Determination of the secondary structures of proteins by circular dichroism and optical rotatory dispersion Biochemistry 11, 4120-4131
55. Qin, Z., Kalinowski, A., Dahl, K. N., and Buehler, M. J. (2011) Structure and stability of the lamin A tail domain and HGPS mutant J. Struct. Biol. 175, 425-433
56. Kapinos, L. E., Burkhard, P., Herrmann, H., Aebi, U., and Strelkov, S. V. (2011) Simultaneous formation of right- and left-handed anti-parallel coiled-coil interfaces by a coil2 fragment of human lamin A J. Mol. Biol. 408, 135-146
57. Taimen, P., Pfleghaar, K., Shimi, T., Moller, D., Ben-Harush, K., Erdos, M. R., Adam, S. A., Herrmann, H., Medalia, O., Collins, F. S., Goldman, A. E., and Goldman, R. D. (2009) A progeria mutation reveals functions for lamin A in nuclear assembly, architecture, and chromosome organization Proc. Natl. Acad. Sci. U.S.A. 106, 20788-20793
58. Lupas, A. N. and Gruber, M. (2005) The structure of α-helical coiled coils Adv. Protein Chem. 70, 37-78
59. Zhou, N. E., Kay, C. M., and Hodges, R. S. (1992) Synthetic model proteins. Positional effects of interchain hydrophobic interactions on stability of two-stranded α-helical coiled-coils J. Biol. Chem. 267, 2664-2670
60. Meier, M., Stetefeld, J., and Burkhard, P. (2010) The many types of interhelical ionic interactions in coiled coils: An overview J. Struct. Biol. 170, 192-201
61. Strelkov, S. V. and Burkhard, P. (2002) Analysis of α-helical coiled coils with the program TWISTER reveals a structural mechanism for stutter compensation J. Struct. Biol. 137, 54-64
62. Strelkov, S. V., Herrmann, H., Geisler, N., Wedig, T., Zimbelmann, R., Aebi, U., and Burkhard, P. (2002) Conserved segments 1A and 2B of the intermediate filament dimer: Their atomic structures and role in filament assembly EMBO J. 21, 1255-1266
63. Cohen, C. and Parry, D. A. D. (1986) α-Helical coiled coils: A widespread motif in proteins Trends Biochem. Sci. 11, 245-248
64. Cohen, C. and Parry, D. A. (1990) α-Helical coiled coils and bundles: How to design an α-helical protein Proteins 7, 1-15
65. Lupas, A. (1996) Prediction and analysis of coiled-coil structures Methods Enzymol. 266, 513-525
66. Lupas, A., Van Dyke, M., and Stock, J. (1991) Predicting coiled coils from protein sequences Science 252, 1162-1164
67. Zwerger, M., Jaalouk, D. E., Lombardi, M. L., Isermann, P., Mauermann, M., Dialynas, G., Herrmann, H., Wallrath, L. L., and Lammerding, J. (2013) Myopathic lamin mutations impair nuclear stability in cells and tissue and disrupt nucleo-cytoskeletal coupling Hum. Mol. Genet. DOI: 10.1093/hmg/ddt079
68. Pasotti, M., Klersy, C., Pilotto, A., Marziliano, N., Rapezzi, C., Serio, A., Mannarino, S., Gambarin, F., Favalli, V., Grasso, M., Agozzino, M., Campana, C., Gavazzi, A., Febo, O., Marini, M., Landolina, M., Mortara, A., Piccolo, G., Vigano, M., Tavazzi, L., and Arbustini, E. (2008) Long-term outcome and risk stratification in dilated cardiolaminopathies J. Am. Coll. Cardiol. 52, 1250-1260