In silico investigation of molecular mechanism of laminopathy caused by a point mutation (R482W) in lamin A/C protein

Amino Acids

Volumn 43, Issue 2, 2012, Pages 603-615

  Rajendran, Vidya ^a   Purohit, Rituraj ^a   Sethumadhavan, Rao ^a  

^a VIT UNIVERSITY   (India)

Author keywords

Docking simulation; Laminopathy; RMSD; SASA

Indexed keywords

EMERIN; HYBRID PROTEIN; LAMIN A; LAMIN A/C PROTEIN; LAMIN C; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; COMPUTER ANALYSIS; COMPUTER PROGRAM; CONTROLLED STUDY; FAMILIAL PARTIAL LIPODYSTROPHY; HYDROGEN BOND; LAMIN A GENE; LAMIN C GENE; LAMINOPATHY; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR MODEL; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

AMINO ACID SUBSTITUTION; HUMANS; HYDROGEN BONDING; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LAMIN TYPE A; LIPODYSTROPHY, FAMILIAL PARTIAL; MEMBRANE PROTEINS; MOLECULAR DYNAMICS SIMULATION; NUCLEAR PROTEINS; PRINCIPAL COMPONENT ANALYSIS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; THERMODYNAMICS;

EID: 84864771186     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-011-1108-7     Document Type: Article

References (74)

1. Amadei A, Linssen ABM, Berendsen HJC (1993) Essential dynamics of proteins. Proteins 17:412-425
2. Araújo-Vilar D, Lattanzi G, González-Méndez B, Costa-Freitas AT, Prieto D, Columbaro M, Mattioli E, Victoria B, Mart?́nez-Sánchez N, Ramazanova A, Fraga M, Beiras A, Forteza J, Dom?́nguez-Gerpe L, Calvo C, Lado-Abeal J (2009) Sitedependent differences in both prelamin A and adipogenic genes in subcutaneous adipose tissue of patients with type 2 familial partial lipodystrophy. J Med Genet 46(1):40-48
3. Bank EM, Ben-Harush K, Wiesel-Motiuk N, Barkan R, Feinstein N, Lotan O, Medalia O, Gruenbaum Y (2011) A laminopathic mutation disrupting lamin filament assembly causes disease-like phenotypes in Caenorhabditis elegans. Mol Biol Cell 22(15): 2716-2728
4. Berendsen HJC, Postma JPM, Gunsteren WFV, Hermans J (1981) Interaction models for water in relation to protein hydration. In: Pullman B (ed) Intermolecular forces. D Reidel Publishing Company, Dordrecht, pp 331-342
5. Berendsen HJC, Postma JPM, DiNola A, Hakk JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81:3684-3690
6. Berman HM, Westbrook JZ, Feng G, Gilliland TN, Bhat H, Weissig IN et al (2000) Nucleic Acids Res 28:235-242
7. Bione S, Maestrini E, Rivella S, Mancini M, Regis S, Romeo G, Toniolo D (1994) Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy. Nat Genet 8:323-327
8. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54:905-921
9. Burke B, Stewart CL (2002) Life at the edge: the nuclear envelope and human disease. Nat Rev Mol Cell Biol 3:575-585
10. Burn J, Baraitser M (1986) Partial lipoatrophy with insulin resistant diabetes and hyperlipidaemia (Dunnigan syndrome). J Med Genet 23:128-130
11. Cao H, Hegele RA (2000) Nuclear lamin A/C R482Q mutation in Canadian kindreds with Dunnigan-type familial partial lipodystrophy. Hum Mol Genet 9:109-112
12. Case DA, Pearlman DA, Caldwell JW, Wang J, Ross WS, Simmerling CL, Darden TA, Mertz KM, Stanton RV, Cheng AL, Vincent JJ, Crowley M, Tsue V, Gohlke H, Radmer R, Duan Y, Pitera J, Massova I, Seibel GL, Singh C, Weiner P, Kollman PA (2002) AMBER simulation software package, version 7, vol 2006. University of California, San Francisco
13. Clements L, Manilal S, Love DR, Morris GE (2000) Direct interaction between emerin and lamin A. Biochem Biophys Res Commun 267:709-714
14. Cohen M, Lee KK, Wilson KL, Gruenbaum Y (2001) Transcriptional repression, apoptosis, human disease and the functional evolution of the nuclear lamina. Trends Biochem Sci 26:41-47
15. de Vries SJ, van Dijk M, Bonvin AMJJ (2010) The HADDOCK web server for data-driven biomolecular docking. Nat Protoc 5:883-897
16. Dhe-Paganon S, Werner ED, Chi YI, Shoelson SE (2002) Structure of the globular tail of nuclear lamin. J Biol Chem 277(20):17381-17384
17. Dominguez C, Boelens R, Bonvin AM (2003) HADDOCK: a protein-protein docking approach based on biochemical or biophysical information. J Am Chem Soc 125:1731-1737
18. Eisenhaber F, Argos P (1996) Hydrophobic regions on protein surfaces: definition based on hydration shell structure and a quick method for their computation. Protein Eng 9(12):1121-1133
19. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr Sect D Biol Crystallogr 60:2126-2132
20. Essmann U, Perera L, Berkowitz ML, Darden T, Lee H, Pedersen LG (1995) A smooth particle mesh Ewald method. J Chem Phys 103:8577-8593
21. Frock RL, Kudlow BA, Evans AM, Jameson SA, Hauschka SD, Kennedy BK (2006) Lamin A/C and emerin are critical for skeletal muscle satellite cell differentiation. Genes Dev 20(4): 486-500
22. Garg A, Peshock RM, Fleckenstein JL (1999) Adipose tissue distribution pattern in patients with familial partial lipodystrophy (Dunnigan variety). J Clin Endocrinol Metab 84:170-174
23. Gunsteren WFV, Billeter SR, Eising AA, Hunenberger PH, Kruger P, Mark AE, Scott WRP, Tironi TG (1996) Biomolecular simulation: the Gromos 96 manual and user guide. Hochschulverlag AG an der Zurich, Zurich
24. Halperin I, Ma B, Wolfson H, Nussinov R (2002) Principles of docking: an overview of search algorithms and a guide to scoring functions. Proteins Struct Funct Genet 47:409-443
25. Hegele RA (2001) Premature atherosclerosis associated with monogenic insulin resistance. Circulation 103:2225-2229
26. Hegele RA, Cao H, Anderson CM, Hramiak IM (2000a) Heterogeneity of nuclear lamin A mutations in Dunnigan-type familial partial lipodystrophy. J Clin Endocrinol Metab 85:3431-3435
27. Hegele RA, Anderson CM, Cao H (2000b) Lamin A/C mutation in a woman and her two daughters with Dunnigan-type partial lipodystrophy and insulin resistance. Diabetes Care 23:258-259
28. Hess B, Kutzner C, Spoel D, Lindahl E (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 4:435-447
29. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14:33-38
30. Jacob KN, Garg A (2006) Laminopathies: multisystem dystrophy syndromes. Mol Genet Metab 87:289-302
31. Janin J, Henrick K, Moult J, Eyck LT, Sternberg MJ, Vajda S, Vakser I, Wodak SJ (2003) CAPRI: a critical assessment of predicted interactions. Proteins Struct Funct Genet 52:2-9
32. Kim JB, Spiegelman BM (1996) ADD1/SREBP1 promotes adipocyte differentiation and gene expression linked to fatty acid metabolism. Genes Dev 10(9):1096-1107
33. Kobberling J, Dunnigan MF (1986) Familial partial lipodystrophy: two types of an X linked dominant syndrome, lethal in the hemizygous state. J Med Genet 23:120-127
34. Lado-Abeal J, Calvo RM, Victoria B, Castro I, Obregon MJ, Araujo-Vilar D (2010) Regional decrease of subcutaneous adipose tissue in patients with type 2 familial partial lipodystrophy is associated with changes in thyroid hormone metabolism. Thyroid. 20(4):419-424
35. Lloyd DJ, Trembath RC, Shackleton S (2002) A novel interaction between lamin A and SREBP1: implications for partial lipodystrophy and other laminopathies. Hum Mol Genet 11:769-777
36. Magracheva E, Kozlov S, Stewart CL, Wlodawer A, Zdanov A (2009) Structure of the lamin A/C R482W mutant responsible for dominant familial partial lipodystrophy (FPLD). Acta Crystallogr Sect F Struct Biol Cryst Commun 65:665-670
37. Manilal S, Man NT, Morris GE (1998) Colocalization of emerin and lamins in interphase nuclei and changes during mitosis. Biochem Biophys Res Commun 249:643-647
38. Manilal S, Sewry CA, Pereboev A (1999) Colocalization of emerin and lamins in interphase nuclei and changes during mitosis. Hum Mol Genet 8:353-359
39. Maraldi NM, Capanni C, Mattioli E, Columbaro M, Squarzoni S, Parnaik WK, Wehnert M, Lattanzi G (2007) A pathogenic mechanism leading to partial lipodystrophy and prospects for pharmacological treatment of insulin resistance syndrome. Acta Biomed 78:207-215
40. Maraldi NM, Capanni C, Cenni V, Fini M, Lattanzi G (2011) Laminopathies and lamin-associated signaling pathways. J Cell Biochem 112(4):979-992
41. McDonald IK, Thornton JM (1994) Satisfying hydrogen bonding potential in proteins. J Mol Biol 238:777-793
42. Newport JW, Wilson KL, Dunphy WG (1990) A lamin-independent pathway for nuclear envelope assembly. J Cell Biol 111:2247-2259
43. 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 (2004) Defects in nuclear structure and function promote dilated cardiomyopathy in lamin A/C-deficient mice. J Clin Invest 113(3):357-369
44. Nilges M (1995) Calculation of protein structures with ambiguous distance restraints. Automated assignment of ambiguous NOE crosspeaks and disulphide connectivities. J Mol Biol 245:645-660
45. Nilges M, Macias MJ, O'Donoghue SI, Oschkinat H (1997) Automated NOESY interpretation with ambiguous distance restraints: the refined NMR solution structure of the pleckstrin homology domain from beta-spectrin. J Mol Biol 269:408-422
46. Ostlund C, Ellenberg J, Hallberg E, Lippincott-Schwartz J, Worman HJ (1999) Intracellular trafficking of emerin, the Emery-Dreifuss muscular dystrophy protein. J Cell Sci 112:1709-1719
47. Ostlund 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
48. Párraga A, Bellsolell L, Ferré-D'Amaré AR, Burley SK (1998) Cocrystal structure of sterol regulatory element binding protein 1a at 2.3 A resolution. Structure 6(5):661-672
49. Prokocimer M, Davidovich M, Nissim-Rafinia M, Wiesel-Motiuk N, Bar DZ, Barkan R, Meshorer E, Gruenbaum Y (2009) Nuclear lamins: key regulators of nuclear structure and activities. J Cell Mol Med 13:1059-1085
50. Purohit R, Sethumadhavan R (2009) Structural Basis for the resilience of darunavir (TMC114) resistance major flap mutations of HIV-1 protease. Interdiscip Sci 1(4):320-328
51. Purohit R, Rajasekaran R, Sudandiradoss C, George Priya Doss C, Ramanathan K, Sethumadhavan R (2008) Studies on flexibility and binding affinity of Asp25 of HIV-1 protease mutants. Int J Biol Macromol 42(4):386-391
52. Purohit R, Rajendran V, Sethumadhavan R (2011a) Relationship between mutation of serine residue at 315th position in M. tuberculosis catalase-peroxidase enzyme and isoniazid susceptibility: an in silico analysis. J Mol Model 17(4):869-877
53. Purohit R, Rajendran V, Sethumadhavan R (2011b) Studies on adaptability of binding residues and flap region of TMC-114 resistance HIV-1 protease mutants. J Biomol Struct Dyn 29(1):137-152
54. Sakaki M, Koike H, Takahashi N, Sasagawa N, Tomioka S, Arahata K, Ishiura S (2001) Interaction between emerin and nuclear lamins. J Biochem 129(2):321-327
55. Schmidt HH, Genschel J, Baier P, Schmidt M, Ockenga J, Tietge UJ, Pröpsting M, Büttner C, Manns MP, Lochs H, Brabant G (2001) Dyslipemia in familial partial lipodystrophy caused by an R482W mutation in the LMNA gene. J Clin Endocrinol Metab 86(5):2289-2295
56. Shackleton S, Lloyd DJ, Jackson SN, Evans R, Niermeijer MF, Singh BM, Schmidt H, Brabant G, Kumar S, Durrington PN, Gregory S, O'Rahilly S, Trembath RC (2000) LMNA, encoding lamin A/C, is mutated in partial lipodystrophy. Nat Genet 24:153-156
57. Speckman RA, Garg A, Du F, Bennett L, Veile R, Arioglu E, Taylor SI, Lovett M, Bowcock AM (2000) Mutational and haplotype analyses of families with familial partial lipodystrophy (Dunnigan variety) reveal recurrent missense mutations in the globular C-terminal domain of lamin A/C. Am J Hum Genet 66:1192-1198
58. Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJ (2005) GROMACS: fast, flexible, and free. J Comput Chem 26:1701-1718
59. Strelkov SV, Herrmann H, Aebi U (2003) Molecular architecture of intermediate filaments. Bioessays 25:243-251
60. Stuurman N, Heins S, Aebi U (1998) Nuclear lamins: their structure, assembly, and interactions. J Struct Biol 122:42-66
61. Sullivan T, Escalante-Alcalde D, Bhatt H, Anver M, Bhat N, Nagashima K, Stewart CL, Burke B (1999) Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 147:913-920
62. Teng S, Madej T, Panchenko A, Alexov E (2009) Modeling effects of human single nucleotide polymorphisms on protein-protein interactions. Biophys J 96(6):2178-2188
63. Tilgner K, Wojciechowicz K, Jahoda C, Hutchison C, Markiewicz E (2009) Dynamic complexes of A-type lamins and emerin influence adipogenic capacity of the cell via nucleocytoplasmic distribution of {beta}-catenin. J Cell Sci 122:401-413
64. Tsuchiya Y, Hase A, Ogawa M, Yorifuji H, Arahata A (1999) Distinct regions specify the nuclear membrane targeting of emerin, the responsible protein for Emery-Dreifuss muscular dystrophy. Eur J Biochem 259:859-886
65. Vallone B, Miele AE, Vecchini P, Chiancone E, Brunori M (1998) Free energy of burying hydrophobic residues in the interface between protein subunits. Proc Natl Acad Sci USA 95:6103-6107
66. Vantyghem MC, Pigny P, Maurage CA, Rouaix-Emery N, Stojkovic T, Cuisset JM, Millaire A, Lascols O, Vermersch P, Wemeau JL, Capeau J, Vigouroux C (2004) Patients with familial partial lipodystrophy of the Dunnigan type due to a LMNA R482W mutation show muscular and cardiac abnormalities. J Clin Endocrinol Metab 89(11):5337-5346
67. Vantyghem MC, Faivre-Defrance F, Marcelli-Tourvieille S, Fermon C, Evrard A, Bourdelle-Hego MF (2007) Familial partial lipodystrophy due to the LMNA R482W mutation with multinodular goitre, extrapyramidal syndrome and primary hyperaldosteronism. Clin Endocrinol (Oxf) 67(2):247-249
68. Vigouroux C, Magré J, Vantyghem MC, Bourut C, Lascols O, Shackleton S, Lloyd DJ, Guerci B, Padova G, Valensi P, Grimaldi A, Piquemal R, Touraine P, Trembath RC, Capeau J (2000) Lamin A/C gene. Sex-determined expression of mutations in Dunnigan-type familial partial lipodystrophy and absence of coding mutations in congenital and acquired generalized lipoatrophy. Diabetes 49:1958-1962
69. 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
70. Wallace AC, Laskowski RA, Thornton JM (1995) LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng 8:127-134
71. Wolff N, Gilquin B, Courchay K, Callebaut I, Worman HJ, Zinn-Justin S (2001) Structural analysis of emerin, an inner nuclear membrane protein mutated in X-linked Emery-Dreifuss muscular dystrophy. FEBS Lett 501(2-3):171-176
72. Yokoyama C, Wang X, Briggs MR, Admon A, Wu J, Hua X, Goldstein JL, Brown MS (1993) SREBP-1, a basic-helix-loophelix-leucine zipper protein that controls transcription of the low density lipoprotein receptor gene. Cell 75(1):187-197
73. Young L, Jernigan RL, Covell DG (1994) A role for surface hydrophobicity in protein-protein recognition. Protein Sci 3(5):717-729
74. Zhang Z, Norris J, Schwartz C, Alexov E (2011) In silico and in vitro investigations of the mutability of disease-causing missense mutation sites in spermine synthase. PLoS One 6(5):e20373