Bioinformatic analysis of pathogenic missense mutations of activin receptor like kinase 1 ectodomain

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Scotti, Claudia ^a   Olivieri, Carla ^a   Boeri, Laura ^a   Canzonieri, Cecilia ^a   Ornati, Federica ^a   Buscarini, Elisabetta ^b   Pagella, Fabio ^c   Danesino, Cesare ^a,c  

^a UNIVERSITY OF PAVIA   (Italy)

^b MAGGIORE HOSPITAL   (Italy)

^c FONDAZIONE IRCCS POLICLINICO SAN MATTEO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN RECEPTOR LIKE KINASE 1; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 9; CYSTINE; ENDOGLIN; TRANSFORMING GROWTH FACTOR BETA1; ACTIVIN RECEPTOR 2; ACVRL1 PROTEIN, HUMAN; GDF2 PROTEIN, HUMAN; GROWTH DIFFERENTIATION FACTOR;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BIOINFORMATICS; HUMAN; HYDROGEN BOND; HYDROPHOBICITY; MISSENSE MUTATION; MOLECULAR DOCKING; MOLECULAR MODEL; MUTATIONAL ANALYSIS; PREDICTION; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; STATIC ELECTRICITY; STEREOCHEMISTRY; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME STABILITY; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOLOGY; PROTEIN TERTIARY STRUCTURE; RENDU OSLER WEBER DISEASE;

ACTIVIN RECEPTORS, TYPE II; AMINO ACID SEQUENCE; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; DNA MUTATIONAL ANALYSIS; ENZYME STABILITY; GROWTH DIFFERENTIATION FACTORS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; STATIC ELECTRICITY; TELANGIECTASIA, HEREDITARY HEMORRHAGIC;

EID: 80054756414     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026431     Document Type: Article

References (108)

1. Shi Y, Massague J, (2003) Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113: 685-700.
2. Massague J, (1998) TGF-beta signal transduction. Annu Rev Biochem 67: 753-791.
3. Bilandzic M, Stenvers KL, (2011) Betaglycan: a multifunctional accessory. Mol Cell Endocrinol 339: 180-189.
4. van Meeteren LA, Goumans MJ, Ten Dijke P, (2011) TGF-beta Receptor Signaling Pathways in Angiogenesis; Emerging Targets for Anti-Angiogenesis Therapy. Curr Pharm Biotechnol.
5. Corradini E, Babitt JL, Lin HY, (2009) The RGM/DRAGON family of BMP co-receptors. Cytokine Growth Factor Rev 20: 389-398.
6. Massague J, (2008) TGFbeta in Cancer. Cell 134: 215-230.
7. Kirsch T, Sebald W, Dreyer MK, (2000) Crystal structure of the BMP-2-BRIA ectodomain complex. Nat Struct Biol 7: 492-496.
8. Greenwald J, Groppe J, Gray P, Wiater E, Kwiatkowski W, et al. (2003) The BMP7/ActRII extracellular domain complex provides new insights into the cooperative nature of receptor assembly. Mol Cell 11: 605-617.
9. Thompson TB, Woodruff TK, Jardetzky TS, (2003) Structures of an ActRIIB:activin A complex reveal a novel binding mode for TGF-beta ligand:receptor interactions. Embo J 22: 1555-1566.
10. ten Dijke P, Yamashita H, Sampath TK, Reddi AH, Estevez M, et al. (1994) Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4. J Biol Chem 269: 16985-16988.
11. David L, Mallet C, Mazerbourg S, Feige JJ, Bailly S, (2007) Identification of BMP9 and BMP10 as functional activators of the orphan activin receptor-like kinase 1 (ALK1) in endothelial cells. Blood 109: 1953-1961.
12. Scharpfenecker M, van Dinther M, Liu Z, van Bezooijen RL, Zhao Q, et al. (2007) BMP-9 signals via ALK1 and inhibits bFGF-induced endothelial cell proliferation and VEGF-stimulated angiogenesis. J Cell Sci 120: 964-972.
13. Brown MA, Zhao Q, Baker KA, Naik C, Chen C, et al. (2005) Crystal structure of BMP-9 and functional interactions with pro-region and receptors. J Biol Chem 280: 25111-25118.
14. David L, Feige JJ, Bailly S, (2009) Emerging role of bone morphogenetic proteins in angiogenesis. Cytokine Growth Factor Rev 20: 203-212.
15. Lin SJ, Lerch TF, Cook RW, Jardetzky TS, Woodruff TK, (2006) The structural basis of TGF-beta, bone morphogenetic protein, and activin ligand binding. Reproduction 132: 179-190.
16. Groppe J, Hinck CS, Samavarchi-Tehrani P, Zubieta C, Schuermann JP, et al. (2008) Cooperative assembly of TGF-beta superfamily signaling complexes is mediated by two disparate mechanisms and distinct modes of receptor binding. Mol Cell 29: 157-168.
17. Govani FS, Shovlin CL, (2009) Hereditary haemorrhagic telangiectasia: a clinical and scientific review. Eur J Hum Genet 17: 860-871.
18. HHT mutation database website. Available: www.hhtmutation.org. Accessed: 2011 Jun 17.
19. Olivieri C, Pagella F, Semino L, Lanzarini L, Valacca C, et al. (2007) Analysis of ENG and ACVRL1 genes in 137 HHT Italian families identifies 76 different mutations (24 novel). Comparison with other European studies. J Hum Genet 52: 820-829.
20. Bross P, Corydon TJ, Andresen BS, Jorgensen MM, Bolund L, et al. (1999) Protein misfolding and degradation in genetic diseases. Hum Mutat 14: 186-198.
21. Ricard N, Bidart M, Mallet C, Lesca G, Giraud S, et al. (2010) Functional analysis of the BMP9 response of ALK1 mutants from HHT2 patients: a diagnostic tool for novel ACVRL1 mutations. Blood 116: 1604-1612.
22. Thusberg J, Vihinen M, (2006) Bioinformatic analysis of protein structure-function relationships: case study of leukocyte elastase (ELA2) missense mutations. Hum Mutat 27: 1230-1243.
23. Lappalainen I, Vihinen M, (2002) Structural basis of ICF-causing mutations in the methyltransferase domain of DNMT3B. Protein Eng 15: 1005-1014.
24. Rong SB, Valiaho J, Vihinen M, (2000) Structural basis of Bloom syndrome (BS) causing mutations in the BLM helicase domain. Mol Med 6: 155-164.
25. Lappalainen I, Giliani S, Franceschini R, Bonnefoy JY, Duckett C, et al. (2000) Structural basis for SH2D1A mutations in X-linked lymphoproliferative disease. Biochem Biophys Res Commun 269: 124-130.
26. Prediction center website. Available: http://predictioncenter.org/casp9/index.cgi. Accessed: 2011 Jun 2017.
27. Bujnicki JM, (2003) Crystallographic and bioinformatic studies on restriction endonucleases: inference of evolutionary relationships in the "midnight zone" of homology. Curr Protein Pept Sci 4: 327-337.
28. Godzik A, (2003) Fold recognition methods. Methods Biochem Anal 44: 525-546.
29. Wallner B, Fang H, Elofsson A, (2003) Automatic consensus-based fold recognition using Pcons, ProQ, and Pmodeller. Proteins 53 (Suppl 6): 534-541.
30. Wallner B, Elofsson A, (2005) Pcons5: combining consensus, structural evaluation and fold recognition scores. Bioinformatics 21: 4248-4254.
31. Wallner B, Elofsson A, (2006) Identification of correct regions in protein models using structural, alignment, and consensus information. Protein Sci 15: 900-913.
32. Tramontano A, (1998) Homology modeling with low sequence identity. Methods 14: 293-300.
33. Rodriguez R, Chinea G, Lopez N, Pons T, Vriend G, (1998) Homology modeling, model and software evaluation: three related resources. Bioinformatics 14: 523-528.
34. Westhead DR, Thornton JM, (1998) Protein structure prediction. Curr Opin Biotechnol 9: 383-389.
35. Kurowski MA, Bujnicki JM, (2003) GeneSilico protein structure prediction meta-server. Nucleic Acids Res 31: 3305-3307.
36. Kosinski J, Cymerman IA, Feder M, Kurowski MA, Sasin JM, et al. (2003) A "FRankenstein's monster" approach to comparative modeling: merging the finest fragments of Fold-Recognition models and iterative model refinement aided by 3D structure evaluation. Proteins 53 (Suppl 6): 369-379.
37. Roy A, Kucukural A, Zhang Y, (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5: 725-738.
38. Peng I, Xu J, A multiple-template approach to protein threading. Submitted to PROTEINS, 2010.
39. Zhang lab website. Available: http://zhanglab.ccmb.med.umich.edu/casp9/14D.html. Accessed: 2011 Jun 17.
40. Fiser A, Sali A, (2003) Modeller: generation and refinement of homology-based protein structure models. Methods Enzymol 374: 461-491.
41. McGuffin LJ, Bryson K, Jones DT, (2000) The PSIPRED protein structure prediction server. Bioinformatics 16: 404-405.
42. Lovell SC, Davis IW, Arendall WB 3rd, de Bakker PI, Word JM, et al. (2003) Structure validation by Calpha geometry: phi,psi and Cbeta deviation. Proteins 50: 437-450.
43. Wiederstein M, Sippl MJ, (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res 35: W407-410.
44. Sippl MJ, (1993) Recognition of errors in three-dimensional structures of proteins. Proteins 17: 355-362.
45. Eisenberg D, Luthy R, Bowie JU, (1997) VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol 277: 396-404.
46. Wallner B, Elofsson A, (2003) Can correct protein models be identified? Protein Sci 12: 1073-1086.
47. Mooney SD, Klein TE, (2002) The functional importance of disease-associated mutation. BMC Bioinformatics 3: 24.
48. Miller MP, Kumar S, (2001) Understanding human disease mutations through the use of interspecific genetic variation. Hum Mol Genet 10: 2319-2328.
49. Shen B, Vihinen M, (2004) Conservation and covariance in PH domain sequences: physicochemical profile and information theoretical analysis of XLA-causing mutations in the Btk PH domain. Protein Eng Des Sel 17: 267-276.
50. Vitkup D, Sander C, Church GM, (2003) The amino-acid mutational spectrum of human genetic disease. Genome Biol 4: R72.
51. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. The Pfam protein families database. Nucleic Acids Res 38: D211-222.
52. MultiDisp website. Available: http://bioinf.uta.fi/cgi-bin/MultiDisp.cgi. Accessed: 2011 Jun 17.
53. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N, (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38: W529-533.
54. ProCon website. Available: http://bioinf.uta.fi/ProCon/instructions.shtml. Accessed: 2011 Jun 17.
55. Schweers O, Schonbrunn-Hanebeck E, Marx A, Mandelkow E, (1994) Structural studies of tau protein and Alzheimer paired helical filaments show no evidence for beta-structure. J Biol Chem 269: 24290-24297.
56. Bates G, (2003) Huntingtin aggregation and toxicity in Huntington's disease. Lancet 361: 1642-1644.
57. Grateau G, Verine J, Delpech M, Ries M, (2005) [Amyloidosis: a model of misfolded protein disorder]. Med Sci (Paris) 21: 627-633.
58. Haigis MC, Yankner BA, (2010) The aging stress response. Mol Cell 40: 333-344.
59. Dosztanyi Z, Magyar C, Tusnady G, Simon I, (2003) SCide: identification of stabilization centers in proteins. Bioinformatics 19: 899-900.
60. Dosztanyi Z, Fiser A, Simon I, (1997) Stabilization centers in proteins: identification, characterization and predictions. J Mol Biol 272: 597-612.
61. Magyar C, Gromiha MM, Pujadas G, Tusnady GE, Simon I, (2005) SRide: a server for identifying stabilizing residues in proteins. Nucleic Acids Res 33: W303-305.
62. Lee B, Richards FM, (1971) The interpretation of protein structures: estimation of static accessibility. J Mol Biol 55: 379-400.
63. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, et al. Overview of the CCP4 suite and current developments. Acta Crystallogr D Biol Crystallogr 67: 235-242.
64. Higa RH, Togawa RC, Montagner AJ, Palandrani JC, Okimoto IK, et al. (2004) STING Millennium Suite: integrated software for extensive analyses of 3d structures of proteins and their complexes. BMC Bioinformatics 5: 107.
65. Runker AE, Bartsch U, Nave KA, Schachner M, (2003) The C264Y missense mutation in the extracellular domain of L1 impairs protein trafficking in vitro and in vivo. J Neurosci 23: 277-286.
66. Ward CL, Kopito RR, (1994) Intracellular turnover of cystic fibrosis transmembrane conductance regulator. Inefficient processing and rapid degradation of wild-type and mutant proteins. J Biol Chem 269: 25710-25718.
67. Cheng SH, Gregory RJ, Marshall J, Paul S, Souza DW, et al. (1990) Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63: 827-834.
68. Mahadeva R, Stewart S, Bilton D, Lomas DA, (1998) Alpha-1 antitrypsin deficiency alleles and severe cystic fibrosis lung disease. Thorax 53: 1022-1024.
69. Bone LJ, Deschenes SM, Balice-Gordon RJ, Fischbeck KH, Scherer SS, (1997) Connexin32 and X-linked Charcot-Marie-Tooth disease. Neurobiol Dis 4: 221-230.
70. Hurtley SM, Helenius A, (1989) Protein oligomerization in the endoplasmic reticulum. Annu Rev Cell Biol 5: 277-307.
71. Thomas PJ, Shenbagamurthi P, Ysern X, Pedersen PL, (1991) Cystic fibrosis transmembrane conductance regulator: nucleotide binding to a synthetic peptide. Science 251: 555-557.
72. Comeau SR, Gatchell DW, Vajda S, Camacho CJ, (2004) ClusPro: an automated docking and discrimination method for the prediction of protein complexes. Bioinformatics 20: 45-50.
73. Scheufler C, Sebald W, Hulsmeyer M, (1999) Crystal structure of human bone morphogenetic protein-2 at 2.7 A resolution. J Mol Biol 287: 103-115.
74. Xu Y, Liu Z, Cai L, Xu D, (2006) Protein Structure Prediction by Protein Threading. In: Xu Y, Xu D, Liang J, editors. Computational Methods for Protein Structure Prediction and Modeling, I, II pp. 389-430.
75. Sali A, Blundell TL, (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815.
76. Benkert P, Kunzli M, Schwede T, (2009) QMEAN server for protein model quality estimation. Nucleic Acids Res 37: W510-514.
77. Shovlin CL, Guttmacher AE, Buscarini E, Faughnan ME, Hyland RH, et al. (2000) Diagnostic criteria for hereditary hemorrhagic telangiectasia (Rendu-Osler-Weber syndrome). Am J Med Genet 91: 66-67.
78. Notredame C, Higgins DG, Heringa J, (2000) T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302: 205-217.
79. Katoh K, Toh H, (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9: 286-298.
80. Pei J, Grishin NV, (2007) PROMALS: towards accurate multiple sequence alignments of distantly related proteins. Bioinformatics 23: 802-808.
81. Higgins DG, Thompson JD, Gibson TJ, (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol 266: 383-402.
82. Edgar RC, (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
83. Ward JJ, Sodhi JS, McGuffin LJ, Buxton BF, Jones DT, (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J Mol Biol 337: 635-645.
84. Dosztanyi Z, Csizmok V, Tompa P, Simon I, (2005) IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 21: 3433-3434.
85. Ishida T, Kinoshita K, (2007) PrDOS: prediction of disordered protein regions from amino acid sequence. Nucleic Acids Res 35: W460-464.
86. Yang ZR, Thomson R, McNeil P, Esnouf RM, (2005) RONN: the bio-basis function neural network technique applied to the detection of natively disordered regions in proteins. Bioinformatics 21: 3369-3376.
87. Li X, Romero P, Rani M, Dunker AK, Obradovic Z, (1999) Predicting Protein Disorder for N-, C-, and Internal Regions. Genome Inform Ser Workshop Genome Inform 10: 30-40.
88. Shimizu K, Hirose S, Noguchi T, (2007) POODLE-S: web application for predicting protein disorder by using physicochemical features and reduced amino acid set of a position-specific scoring matrix. Bioinformatics 23: 2337-2338.
89. 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.
90. Linding R, Schymkowitz J, Rousseau F, Diella F, Serrano L, (2004) A comparative study of the relationship between protein structure and beta-aggregation in globular and intrinsically disordered proteins. J Mol Biol 342: 345-353.
91. Trovato A, Seno F, Tosatto SC, (2007) The PASTA server for protein aggregation prediction. Protein Eng Des Sel 20: 521-523.
92. Maurer-Stroh S, Debulpaep M, Kuemmerer N, Lopez de la Paz M, Martins IC, et al. (2010) Exploring the sequence determinants of amyloid structure using position-specific scoring matrices. Nat Methods 7: 237-242.
93. Conchillo-Sole O, de Groot NS, Aviles FX, Vendrell J, Daura X, et al. (2007) AGGRESCAN: a server for the prediction and evaluation of "hot spots" of aggregation in polypeptides. BMC Bioinformatics 8: 65.
94. Kumar P, Henikoff S, Ng PC, (2009) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 4: 1073-1081.
95. Ramensky V, Bork P, Sunyaev S, (2002) Human non-synonymous SNPs: server and survey. Nucleic Acids Res 30: 3894-3900.
96. Guerois R, Nielsen JE, Serrano L, (2002) Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations. J Mol Biol 320: 369-387.
97. Capriotti E, Calabrese R, Casadio R, (2006) Predicting the insurgence of human genetic diseases associated to single point protein mutations with support vector machines and evolutionary information. Bioinformatics 22: 2729-2734.
98. Kwasigroch JM, Gilis D, Dehouck Y, Rooman M, (2002) PoPMuSiC, rationally designing point mutations in protein structures. Bioinformatics 18: 1701-1702.
99. Schymkowitz J, Borg J, Stricher F, Nys R, Rousseau F, et al. (2005) The FoldX web server: an online force field. Nucleic Acids Res 33: W382-388.
100. Zhou H, Zhou Y, (2002) Distance-scaled, finite ideal-gas reference state improves structure-derived potentials of mean force for structure selection and stability prediction. Protein Sci 11: 2714-2726.
101. Parthiban V, Gromiha MM, Abhinandan M, Schomburg D, (2007) Computational modeling of protein mutant stability: analysis and optimization of statistical potentials and structural features reveal insights into prediction model development. BMC Struct Biol 7: 54.
102. 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.
103. Cheng J, Randall A, Baldi P, (2006) Prediction of protein stability changes for single-site mutations using support vector machines. Proteins 62: 1125-1132.
104. Huang LT, Gromiha MM, Ho SY, (2007) iPTREE-STAB: interpretable decision tree based method for predicting protein stability changes upon mutations. Bioinformatics 23: 1292-1293.
105. Yin S, Ding F, Dokholyan NV, (2007) Eris: an automated estimator of protein stability. Nat Methods 4: 466-467.
106. DeLano WL, (2002) The PyMol Molecular Graphics System; In: Scientific D, editors. Palo Alto, CA, USA.
107. Chen R, Li L, Weng Z, (2003) ZDOCK: an initial-stage protein-docking algorithm. Proteins 52: 80-87.
108. Krissinel E, Henrick K, (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372: 774-797.