A computational model of the LGI1 protein suggests a common binding site for ADAM proteins

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Leonardi, Emanuela ^a   Andreazza, Simonetta ^a   Vanin, Stefano ^a,b   Busolin, Giorgia ^c   Nobile, Carlo ^c   Tosatto, Silvio C E ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF HUDDERSFIELD   (United Kingdom)

^c CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM PROTEIN; BRAIN PROTEIN; LEUCINE RICH GLIOMA INACTIVATED 1 PROTEIN; UNCLASSIFIED DRUG; LEUCINE RICH REPEAT PROTEINS; LEUCINE-RICH REPEAT PROTEINS; LGI1 PROTEIN, HUMAN; LIGAND; PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; COMPUTER MODEL; CONTROLLED STUDY; GENE; GENE MUTATION; GLYCOSYLATION; LGI1 GENE; MISSENSE MUTATION; NONHUMAN; PHYLOGENY; PREDICTION; PROTEIN BINDING; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; METHODOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY;

ADAM PROTEINS; AMINO ACID SEQUENCE; BINDING SITES; COMPUTATIONAL BIOLOGY; EVOLUTION, MOLECULAR; GLYCOSYLATION; HUMANS; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PHYLOGENY; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 79953202854     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018142     Document Type: Article

References (64)

1. Kunapuli P, Chitta KS, Cowell JK, (2003) Suppression of the cell proliferation and invasion phenotypes in glioma cells by the LGI1 gene. Oncogene 22: 3985-3991.
2. Kunapuli P, Kasyapa CS, Hawthorn L, Cowell JK, (2004) LGI1, a putative tumor metastasis suppressor gene, controls in vitro invasiveness and expression of matrix metalloproteinases in glioma cells through the ERK1/2 pathway. J Biol Chem 279: 23151-23157.
3. Michelucci R, Poza JJ, Sofia V, de Feo MR, Binelli S, et al. (2003) Autosomal dominant lateral temporal epilepsy: clinical spectrum, new epitempin mutations, and genetic heterogeneity in seven European families. Epilepsia 44: 1289-1297.
4. Ottman R, Risch N, Hauser WA, Pedley TA, Lee JH, et al. (1995) Localization of a gene for partial epilepsy to chromosome 10q. Nat Genet 10: 56-60.
5. Morante-Redolat JM, Gorostidi-Pagola A, Piquer-Sirerol S, Saenz A, Poza JJ, et al. (2002) Mutations in the LGI1/Epitempin gene on 10q24 cause autosomal dominant lateral temporal epilepsy. Hum Mol Genet 11: 1119-1128.
6. Kalachikov S, Evgrafov O, Ross B, Winawer M, Barker-Cummings C, et al. (2002) Mutations in LGI1 cause autosomal-dominant partial epilepsy with auditory features. Nat Genet 30: 335-341.
7. Nobile C, Michelucci R, Andreazza S, Pasini E, Tosatto SC, et al. (2009) LGI1 mutations in autosomal dominant and sporadic lateral temporal epilepsy. Hum Mutat 30: 530-536.
8. Senechal KR, Thaller C, Noebels JL, (2005) ADPEAF mutations reduce levels of secreted LGI1, a putative tumor suppressor protein linked to epilepsy. Hum Mol Genet 14: 1613-1620.
9. Kobe B, Kajava AV, (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11: 725-732.
10. Staub E, Perez-Tur J, Siebert R, Nobile C, Moschonas NK, et al. (2002) The novel EPTP repeat defines a superfamily of proteins implicated in epileptic disorders. Trends Biochem Sci 27: 441-444.
11. Scheel H, Tomiuk S, Hofmann K, (2002) A common protein interaction domain links two recently identified epilepsy genes. Hum Mol Genet 11: 1757-1762.
12. Paoli M, (2001) An elusive propeller-like fold. Nat Struct Biol 8: 744-745.
13. Buchanan SG, Gay NJ, (1996) Structural and functional diversity in the leucine-rich repeat family of proteins. Prog Biophys Mol Biol 65: 1-44.
14. Fukata Y, Adesnik H, Iwanaga T, Bredt DS, Nicoll RA, et al. (2006) Epilepsy-related ligand/receptor complex LGI1 and ADAM22 regulate synaptic transmission. Science 313: 1792-1795.
15. Zhou YD, Lee S, Jin Z, Wright M, Smith SE, et al. (2009) Arrested maturation of excitatory synapses in autosomal dominant lateral temporal lobe epilepsy. Nat Med 15: 1208-1214.
16. Owuor K, Harel NY, Englot DJ, Hisama F, Blumenfeld H, et al. (2009) LGI1-associated epilepsy through altered ADAM23-dependent neuronal morphology. Mol Cell Neurosci 42: 448-457.
17. Fukata Y, Lovero KL, Iwanaga T, Watanabe A, Yokoi N, et al. (2010) Disruption of LGI1-linked synaptic complex causes abnormal synaptic transmission and epilepsy. Proc Natl Acad Sci U S A 107: 3799-3804.
18. Boeckmann B, Bairoch A, Apweiler R, Blatter MC, Estreicher A, et al. (2003) The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res 31: 365-370.
19. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
20. Clamp M, Cuff J, Searle SM, Barton GJ, (2004) The Jalview Java alignment editor. Bioinformatics 20: 426-427.
21. Gouet P, Courcelle E, Stuart DI, Metoz F, (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15: 305-308.
22. Albrecht M, Tosatto SC, Lengauer T, Valle G, (2003) Simple consensus procedures are effective and sufficient in secondary structure prediction. Protein Eng 16: 459-462.
23. Vullo A, Bortolami O, Pollastri G, Tosatto SC, (2006) Spritz: a server for the prediction of intrinsically disordered regions in protein sequences using kernel machines. Nucleic Acids Res 34: W164-168.
24. Bendtsen JD, Nielsen H, von Heijne G, Brunak S, (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
25. Marsella L, Sirocco F, Trovato A, Seno F, Tosatto SC, (2009) REPETITA: detection and discrimination of the periodicity of protein solenoid repeats by discrete Fourier transform. Bioinformatics 25: i289-295.
26. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
27. Strimmer K, Goldman N, von Haeseler A, (1997) Bayesian probabilities and quartet puzzling. Molecular Biology and Evolution 14: 210-211.
28. Strimmer K, von Haeseler A, (1996) Quartet puzzling: A quartet maximum-likelihood method for reconstructing tree topologies. Molecular Biology and Evolution 13: 964-969.
29. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
30. Jones DT, Taylor WR, Thornton JM, (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8: 275-282.
31. Felsenstein J, (1985) Phylogenies and the comparative method. Amer Naturalist 125: 1-15.
32. Bindewald E, Cestaro A, Hesser J, Heiler M, Tosatto SC, (2003) MANIFOLD: protein fold recognition based on secondary structure, sequence similarity and enzyme classification. Protein Eng 16: 785-789.
33. Bujnicki JM, Elofsson A, Fischer D, Rychlewski L, (2001) Structure prediction meta server. Bioinformatics 17: 750-751.
34. Sommer I, Toppo S, Sander O, Lengauer T, Tosatto SC, (2006) Improving the quality of protein structure models by selecting from alignment alternatives. BMC Bioinformatics 7: 364.
35. Perry J, Kleckner N, Borner GV, (2005) Bioinformatic analyses implicate the collaborating meiotic crossover/chiasma proteins Zip2, Zip3, and Spo22/Zip4 in ubiquitin labeling. Proc Natl Acad Sci U S A 102: 17594-17599.
36. Kajava AV, Kobe B, (2002) Assessment of the ability to model proteins with leucine-rich repeats in light of the latest structural information. Protein Sci 11: 1082-1090.
37. Tosatto SC, Bindewald E, Hesser J, Manner R, (2002) A divide and conquer approach to fast loop modeling. Protein Eng 15: 279-286.
38. Canutescu AA, Shelenkov AA, Dunbrack RL, (2003) A graph-theory algorithm for rapid protein side-chain prediction. Protein Science 12: 2001-2014.
39. Tosatto SC, (2005) The Victor/FRST Function for Model Quality Estimation. J Comput Biol 12: 1316-1327.
40. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, et al. (2005) GROMACS: fast, flexible, and free. J Comput Chem 26: 1701-1718.
41. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA, (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98: 10037-10041.
42. Benkert P, Tosatto SC, Schomburg D, (2008) QMEAN: A comprehensive scoring function for model quality assessment. Proteins 71: 261-277.
43. Benkert P, Tosatto SC, Schwede T, (2009) Global and local model quality estimation at CASP8 using the scoring functions QMEAN and QMEANclust. Proteins 77 (Suppl 9): 173-180.
44. Landau M, Mayrose I, Rosenberg Y, Glaser F, Martz E, et al. (2005) ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res 33: W299-302.
45. Capriotti E, Fariselli P, Casadio R, (2005) I-Mutant2.0: predicting stability changes upon mutation from the protein sequence or structure. Nucleic Acids Res 33: W306-310.
46. Cheng J, Randall A, Baldi P, (2006) Prediction of protein stability changes for single-site mutations using support vector machines. Proteins 62: 1125-1132.
47. Yin S, Ding F, Dokholyan NV, (2007) Eris: an automated estimator of protein stability. Nat Methods 4: 466-467.
48. Gilis D, Rooman M, (2000) PoPMuSiC, an algorithm for predicting protein mutant stability changes: application to prion proteins. Protein Eng 13: 849-856.
49. Herranz-Perez V, Olucha-Bordonau FE, Morante-Redolat JM, Perez-Tur J, (2010) Regional distribution of the leucine-rich glioma inactivated (LGI) gene family transcripts in the adult mouse brain. Brain Res 1307: 177-194.
50. Gu W, Gibert Y, Wirth T, Elischer A, Bloch W, et al. (2005) Using gene-history and expression analyses to assess the involvement of LGI genes in human disorders. Mol Biol Evol 22: 2209-2216.
51. Matsushima N, Tachi N, Kuroki Y, Enkhbayar P, Osaki M, et al. (2005) Structural analysis of leucine-rich-repeat variants in proteins associated with human diseases. Cell Mol Life Sci 62: 2771-2791.
52. Howitt JA, Clout NJ, Hohenester E, (2004) Binding site for Robo receptors revealed by dissection of the leucine-rich repeat region of Slit. Embo J 23: 4406-4412.
53. Kobe B, Kajava AV, (2000) When protein folding is simplified to protein coiling: the continuum of solenoid protein structures. Trends Biochem Sci 25: 509-515.
54. Evdokimov AG, Anderson DE, Routzahn KM, Waugh DS, (2001) Unusual molecular architecture of the Yersinia pestis cytotoxin YopM: a leucine-rich repeat protein with the shortest repeating unit. J Mol Biol 312: 807-821.
55. Chaudhuri I, Soding J, Lupas AN, (2008) Evolution of the beta-propeller fold. Proteins 71: 795-803.
56. Smith TF, Gaitatzes C, Saxena K, Neer EJ, (1999) The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24: 181-185.
57. Bella J, Hindle KL, McEwan PA, Lovell SC, (2008) The leucine-rich repeat structure. Cell Mol Life Sci 65: 2307-2333.
58. Kobe B, Deisenhofer J, (1995) A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature 374: 183-186.
59. Stirnimann CU, Petsalaki E, Russell RB, Muller CW, (2010) WD40 proteins propel cellular networks. Trends Biochem Sci.
60. Sagane K, Ishihama Y, Sugimoto H, (2008) LGI1 and LGI4 bind to ADAM22, ADAM23 and ADAM11. Int J Biol Sci 4: 387-396.
61. Ozkaynak E, Abello G, Jaegle M, van Berge L, Hamer D, et al. (2010) Adam22 is a major neuronal receptor for Lgi4-mediated Schwann cell signaling. J Neurosci 30: 3857-3864.
62. Sirerol-Piquer MS, Ayerdi-Izquierdo A, Morante-Redolat JM, Herranz-Perez V, Favell K, et al. (2006) The epilepsy gene LGI1 encodes a secreted glycoprotein that binds to the cell surface. Hum Mol Genet 15: 3436-3445.
63. Chernova OB, Somerville RP, Cowell JK, (1998) A novel gene, LGI1, from 10q24 is rearranged and downregulated in malignant brain tumors. Oncogene 17: 2873-2881.
64. Kiel C, Beltrao P, Serrano L, (2008) Analyzing protein interaction networks using structural information. Annu Rev Biochem 77: 415-441.