Testing computational prediction of missense mutation phenotypes: Functional characterization of 204 mutations of human cystathionine beta synthase

Proteins: Structure, Function and Bioinformatics

Volumn 78, Issue 9, 2010, Pages 2058-2074

  Wei, Qiong ^a   Wang, Liqun ^a   Wang, Qiang ^a   Kruger, Warren D ^a   Dunbrack Jr , Roland L ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

Cystathionine beta synthase; Mutations; Phenotype prediction

Indexed keywords

CYSTATHIONINE; CYSTATHIONINE BETA LYASE; HOMOCYSTEINE; MONOMER; SERINE; TAQ POLYMERASE; CYSTATHIONINE BETA SYNTHASE; CYSTEINE; LAC REPRESSOR;

ANALYTIC METHOD; ANALYZER; ARTICLE; CATALYSIS; CELL GROWTH; COMPUTER PROGRAM; ENZYME ANALYSIS; FUNGAL STRAIN; HUMAN; KERNEL METHOD; MISSENSE MUTATION; MUTAGENESIS; MUTATIONAL ANALYSIS; PHENOTYPE; POLYMERASE CHAIN REACTION; PREDICTION; PRIORITY JOURNAL; PROTEIN DOMAIN; WILD TYPE; YEAST; ALGORITHM; ARTIFICIAL INTELLIGENCE; BIOLOGY; CHEMISTRY; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; PROCEDURES; PROTEIN DATABASE; REPRODUCIBILITY; STATISTICAL MODEL;

ALGORITHMS; ARTIFICIAL INTELLIGENCE; COMPUTATIONAL BIOLOGY; CYSTATHIONINE BETA-SYNTHASE; CYSTEINE; DATABASES, PROTEIN; GENETIC COMPLEMENTATION TEST; HUMANS; LAC REPRESSORS; MODELS, STATISTICAL; MUTAGENESIS; MUTATION, MISSENSE; PHENOTYPE; REPRODUCIBILITY OF RESULTS; YEASTS;

EID: 77953602809     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22722     Document Type: Article

References (92)

1. Collins FS, Patrinos A, Jordan E, Chakravarti A, Gesteland R, Walters L. New goals for the U.S. human genome project: 1998-2003. Science 1998; 282: 682-689.
2. Manolio TA, Collins FS. The HapMap and genome-wide association studies in diagnosis and therapy. Annu Rev Med 2009; 60: 443-456.
3. Carlson KM, Dou S, Chi D, Scavarda N, Toshima K, Jackson CE, Wells SA, Jr, Goodfellow PJ, Donis-Keller H. Single missense mutation in the tyrosine kinase catalytic domain of the RET protooncogene is associated with multiple endocrine neoplasia type 2B. Proc Natl Acad Sci USA 1994; 91: 1579-1583.
4. Garrigue-Antar L, Munoz-Antonia T, Antonia SJ, Gesmonde J, Vellucci VF, Reiss M. Missense mutations of the transforming growth factor beta type II receptor in human head and neck squamous carcinoma cells. Cancer Res 1995; 55: 3982-3987.
5. Marchese CA, Bertolino F, Ceccopieri B, Vanzetti M, Scaglione D, Locatelli L, Montera M, Romio L, Resta N, Stella A, Guanti G, Mareni C. Clinical findings in a family with familial adenomatous polyposis and a missense mutation of the adenomatous polyposis coli gene. Scand J Gastroenterol 1996; 31: 917-920.
6. Wang Y, Friedl W, Lamberti C, Ruelfs C, Kruse R, Propping P. Hereditary nonpolyposis colorectal cancer: causative role of a germline missense mutation in the hMLH1 gene confirmed by the independent occurrence of the same somatic mutation in tumour tissue. Hum Genet 1997; 100: 362-364.
7. Shen D, Wu Y, Chillar R, Vadgama JV. Missense alterations of BRCA1 gene detected in diverse cancer patients. Anticancer Res 2000; 20: 1129-1132.
8. Puxeddu E, Moretti S, Elisei R, Romei C, Pascucci R, Martinelli M, Marino C, Avenia N, Rossi ED, Fadda G, Cavaliere A, Ribacchi R, Falorni A, Pontecorvi A, Pacini F, Pinchera A, Santeusanio F. BRAF(V599E) mutation is the leading genetic event in adult sporadic papillary thyroid carcinomas. J Clin Endocrinol Metab 2004; 89: 2414-2420.
9. Kraus JP, Janosik M, Kozich V, Mandell R, Shih V, Sperandeo MP, Sebastio G, de Franchis R, Andria G, Kluijtmans LA, Blom H, Boers GH, Gordon RB, Kamoun P, Tsai MY, Kruger WD, Koch HG, Ohura T, Gaustadnes M. Cystathionine beta-synthase mutations in homocystinuria. Hum Mutat 1999; 13: 362-375.
10. Huang CN, Lee KC, Wu HP, Tai TY, Lin BJ, Chuang LM. Screening for the Gly40Ser mutation in the glucagon receptor gene among patients with type 2 diabetes or essential hypertension in Taiwan. Pancreas 1999; 18: 151-155.
11. Miller SP, Anand GR, Karschnia EJ, Bell GI, LaPorte DC, Lange AJ. Characterization of glucokinase mutations associated with maturityonset diabetes of the young type 2 (MODY-2): different glucokinase defects lead to a common phenotype. Diabetes 1999; 48: 1645-1651.
12. Macfarlane WM, Frayling TM, Ellard S, Evans JC, Allen LI, Bulman MP, Ayres S, Shepherd M, Clark P, Millward A, Demaine A, Wilkin T, Docherty K, Hattersley AT. Missense mutations in the insulin promoter factor-1 gene predispose to type 2 diabetes. J Clin Invest 1999; 104: R33-R39.
13. Hughes DJ, Hill AJ, Macek M, Jr, Redmond AO, Nevin NC, Graham CA. Mutation characterization of CFTR gene in 206 Northern Irish CF families: thirty mutations, including two novel, account for approximately 94% of CF chromosomes. Hum Mutat 1996; 8: 340-347.
14. Besancon R, Lorenzi A, Cruts M, Radawiec S, Sturtz F, Broussolle E, Chazot G, van Broeckhoven C, Chamba G, Vandenberghe A. Missense mutation in exon 11 (Codon 378) of the presenilin-1 gene in a French family with early-onset Alzheimer's disease and transmission study by mismatch enhanced allele specific amplification. Mutations in brief no. 141. Online. besancon@rockefeller1. univ.lyon1.fr. Hum Mutat 1998; 11: 481.
15. Murayama O, Murayama M, Honda T, Sun X, Nihonmatsu N, Takashima A. Twenty-nine missense mutations linked with familial Alzheimer's disease alter the processing of presenilin 1. Prog Neuropsychopharmacol Biol Psychiatry 1999; 23: 905-913.
16. Campion D, Dumanchin C, Hannequin D, Dubois B, Belliard S, Puel M, Thomas-Anterion C, Michon A, Martin C, Charbonnier F, Raux G, Camuzat A, Penet C, Mesnage V, Martinez M, ClergetDarpoux P, Brice A, Frebourg T. Early-onset autosomal dominant Alzheimer disease: prevalence, genetic heterogeneity, and mutation spectrum. Am J Hum Genet 1999; 65: 664-670.
17. Cooper DN, Ball EV, Krawczak M. The human gene mutation database. Nucleic Acids Res 1998; 26: 285-287.
18. Stenson PD, Ball EV, Mort M, Phillips AD, Shiel JA, Thomas NS, Abeysinghe S, Krawczak M, Cooper DN. Human gene mutation database (HGMD): 2003 update. Hum Mutat 2003; 21: 577-581.
19. Birney E, Andrews D, Bevan P, Caccamo M, Cameron G, Chen Y, Clarke L, Coates G, Cox T, Cuff J, Curwen V, Cutts T, Down T, Durbin R, Eyras E, Pernandez-Suarez XM, Gane P, Gibbins B, Gilbert J, Hammond M, Hotz H, Iyer V, Kahari A, Jekosch K, Kasprzyk A, Keefe D, Keenan S, Lehvaslaiho H, McVicker G, Melsopp C, Meidl P, Mongin E, Pettett R, Potter S, Proctor G, Rae M, Searle S, Slater G, Smedley D, Smith J, Spooner W, Stabenau A, Stalker J, Storey R, Ureta-Vidal A, Woodwark C, Clamp M, Hubbard T. Ensembl 2004. Nucleic Acids Res 2004; 32: D468-D470.
20. Sherry ST, Ward MH, Kholodov M, Baker J, Phan L, Smigielski EM, Sirotkin K. dbSNP: the NCBI database of genetic variation. Nucleic Acids Res 2001; 29: 308-311.
21. Zhao H, Pfeiffer R, Gail MH. Haplotype analysis in population genetics and association studies. Pharmacogenomics 2003; 4: 171-178.
22. Salisbury BA, Pungliya M, Choi JY, Jiang R, Sun XJ, Stephens JC. SNP and haplotype variation in the human genome. Mutat Res 2003; 526: 53-61.
23. Matthews BW. Studies on protein stability with T4 lysozyme. Adv Protein Chem 1995; 46: 249-278.
24. Rennell D, Bouvier SE, Hardy LW, Poteete AR. Systematic mutation of bacteriophage T4 lysozyme. J Mol Biol 1991; 222: 67-88.
25. Shortle D, Meeker AK. Mutant forms of staphylococcal nuclease with altered patterns of guanidine hydrochloride and urea denaturation. Proteins: Struct Funct Genet 1986; 1: 81-89.
26. Green SM, Meeker AK, Shortle D. Contributions of the polar, uncharged amino acids to the stability of staphylococcal nuclease: evidence for mutational effects on the free energy of the denatured state. Biochemistry 1992; 31: 5717-5728.
27. Stites WE, Meeker AK, Shortle D. Evidence for strained interactions between side-chains and the polypeptide backbone. J Mol Biol 1994; 235: 27-32.
28. Meeker AK, Garcia-Moreno B, Shortle D. Contributions of the ionizable amino acids to the stability of staphylococcal nuclease. Biochemistry 1996; 35: 6443-6449.
29. Loeb DD, Swaustrom R, Everitt L, Manchester M, Stamper SE, Hutchison CA, III. Complete mutagenesis of the HIV-1. protease. Nature 1989; 340: 397-400.
30. Axe DD, Foster NW, Fersht AR. Active barnase variants with completely random hydrophobic cores. Proc Natl Acad Sci USA 1996; 93: 5590-5594.
31. Markiewicz P, Kleina LG, Cruz C, Ehret S, Miller JH. Genetic studies of the lac repressor. XIV. Analysis of 4000 altered Escherichia coli lac repressors reveals essential and non-essential residues, as well as "spacers" which do not require a specific sequence. J Mol Biol 1994; 240: 421-433.
32. Schmitz A, Schmeissner U, Miller JH. Mutations affecting the quaternary structure of the lac repressor. J Biol Chem 1976; 251: 3359-3366.
33. Kleina LG, Miller JH. Genetic studies of the lac repressor. XIII. Extensive amino acid replacements generated by the use of natural and synthetic nonsense suppressors. J Mol Biol 1990; 212: 295-318.
34. Suckow J, Markiewicz P, Kleina LG, Miller J, Kisters-Woike B, Muller-Hill B. Genetic studies of the Lac repressor. XV: 4000 single amino acid substitutions and analysis of the resulting phenotypes on the basis of the protein structure. J Mol Biol 1996; 261: 509-523.
35. Pace HC, Kercher MA, Lu P, Markiewicz P, Miller JH, Chang G, Lewis M. Lac repressor genetic map in real space. Trends Biochem. Sci 1997; 22: 334-339.
36. Lewis M, Chang G, Horton NC, Kercher MA, Pace HC, Schumacher MA, Brennan RG, Lu P. Crystal structure of the lactose Operon repressor and its complexes with DNA and inducer. Science 1996; 271: 1247-1254.
37. Bell CE, Lewis M. A closer view of the conformation of the Lac repressor bound to operator. Nat Struct Biol 2000; 7: 209-214.
38. Ng PC, Henikoff S. SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res 2003; 31: 3812-3814.
39. Ng PC, Henikoff S. Accounting for human polymorphisms predicted to affect protein function. Genome Res 2002; 12: 436-446.
40. Ng PC, Henikoff S. Predicting deleterious amino acid substitutions. Genome Res 2001; 11: 863-874.
41. Ramensky V, Bork P, Sunyaev S. Human non-synonymous SNPs: server and survey. Nucleic Acids Res 2002; 30: 3894-3900.
42. Yue P, Li Z, Moult J. Loss of protein structure stability as a major causative factor in monogenic disease. J Mol Biol 2005; 353: 459-473.
43. Yue P, Moult J. Identification and analysis of deleterious human SNPs. J Mol Biol 2006; 356: 1263-1274.
44. Ferrer-Costa C, Orozco M, de la Cruz X. Characterization of disease-associated single amino acid polymorphisms in terms of sequence and structure properties. J Mol Biol 2002; 315: 771-786.
45. Ferrer-Costa C, Orozco M, de la Cruz X. Sequence-based prediction of pathological mutations. Proteins 2004; 57: 811-819.
46. Ferrer-Costa C, Gelpi JL, Zamakola L, Parraga I, de la Cruz X, Orozco M. PMUT: a web-based tool for the annotation of pathological mutations on proteins. Bioinformatics 2005; 21: 3176-3178.
47. Capriotti E, Calabrese R, Casadio R. Predicting the insurgeuce of human genetic diseases associated to single point protein mutations with support vector machines and evolutionary information. Bioinformatics 2006; 22: 2729-2734.
48. Bao L, Cui Y. Prediction of the phenotypic effects of non-synonymous single nucleotide polymorphisms using structural and evolutionary information. Bioinformatics 2005; 21: 2185-2190.
49. Bao L, Zhou M, Cui Y. nsSNPAnalyzer: identifying disease-associated nonsynonymous single nucleotide polymorphisms. Nucleic Acids Res 2005; 33(Web Server issue): W480-W482.
50. Jhee KH, Kruger WD. The role of cystathionine beta-synthase in homocysteine metabolism. Antioxid Redox Signal 2005; 7: 813-822.
51. Mudd SH, Levy HL, Kraus JP. Disorders in transsulfuration In: Scriver CR, Beaudet A, Sly W, Valle D, editors. The metabolic basis of inherited disease. New York: McGraw-Hill; 2001. pp 2007-2056.
52. De Franchis R, Sperandeo MP, Sebastio G, Andria G. Clinical aspects of cystathionine beta-synthase deficiency: how wide is the spectrum? The Italian collaborative study group on homocystinuria. Eur J Pediatrics 1998;157 (Suppl 2): S67-S70.
53. Shan X, Kruger WD. Correction of disease-causing CBS mutations in yeast. Nat Genet 1998; 19: 91-93.
54. Kruger WD, Cox DR. A yeast assay for functional detection of mutations in the human cystathionine beta-synthase gene. Hum Mol Genet 1995; 4: 1155-1161.
55. Matthews BW. Comparison of the predicted and observed secondary structure of T4 phage lysozyme. Biochim Biophys Acta 1975; 405: 442-451.
56. Baldi P, Brunak S, Chauvin Y, Andersen CA, Nielsen H. Assessing the accuracy of prediction algorithms for classification: an overview. Bioinformatics 2000; 16: 412-424.
57. Breiman L. Random forests. Mach Learn 2001; 35: 5-32.
58. Altschul SF, Madden TL, Schärfer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of database programs. Nucleic Acids Res 1997; 25: 3389-3402.
59. Wheeler DL, Barrett T, Benson DA, Bryant SH, Canese K, Chetvernin V, Church DM, Dicuccio M, Edgar R, Federhen S, Feolo M, Geer LY, Helmberg W, Kapustin Y, Khovayko O, Landsman D, Lipman DJ, Madden TL, Maglott DR, Miller V, Ostell J, Pruitt KD, Schuler GD, Shumway M, Sequeira E, Sherry ST, Sirotkin K, Souvorov A, Starchenko G, Tatusov RL, Tatusova TA, Wagner L, Yaschenko E. Database resources of the national center for biotechnology information. Nucleic Acids Res 2008; 36: D13-D21.
60. Hubbard SJ, Thornton JM. NACCESS. London: Department of Biochemistry and Molecular Biology, University College London; 1993.
61. Silverman BW. Density estimation for statistics and data analysis. New York: Chapman & Hall; 1986. 175p.
62. Hall P, Kang KH. Bandwidth choice for nonparametric classification. Ann Stat 2005; 33: 284-306.
63. Kery V, Poneleit L, Kraus JP. Trypsin cleavage of human cystathionine beta-synthase into an evolutionarily conserved active core: structural and functional consequences. Arch Biochem Biophys 1998; 355: 222-232.
64. Shan X, Dunbrack RL, Jr, Christopher SA, Kruger WD. Mutations in the regulatory domain of cystathionine beta-synthase can functionally suppress patient-derived mutations in cis. Hum Mol Genet 2001; 10: 635-643.
65. Meier M, Janosik M, Kery V, Kraus JP, Burkhard P. Structure of human cystathionine beta-synthase: a unique pyridoxal 5′-phosphate-dependent heme protein. EMBO J 2001; 20: 3910-3916.
66. Taoka S, Lepore BW, Kabil O, Ojha S, Ringe D, Banerjee R. Human cystathionine beta-synthase is a heme sensor protein. Evidence that the redox sensor is heme and not the vicinal cysteines in the CXXC motif seen in the crystal structure of the truncated enzyme. Biochemistry 2002; 41: 10454-10461.
67. Kim CE, Gallagher PM, Guttormsen AB, Refsum H, Ueland PM, Ose L, Foiling I, Whitehead AS, Tsai MY, Kruger WD. Functional modeling of vitamin responsiveness in yeast: a common pyridoxine-responsive cystathionine beta-synthase mutation in homocystinuria. Hum Mol Genet 1997; 6: 2213-2221.
68. Shan X, Dunbrack RL, Jr, Christopher SA, Kruger WD. Mutations in the regulatory domain of cystathionine beta synthase can functionally suppress patient-derived mutations in cis. Hum Mol Genet 2001; 10: 635-643.
69. Kruger WD, Wang L, Jhee KH, Singh RH, Elsas LJ, II. Cystathionine beta-synthase deficiency in Georgia (USA): correlation of clinical and biochemical phenotype with genotype. Hum Mutat 2003; 22: 434-441.
70. Minnick DT, Liu L, Grindley ND, Kunkel TA, Joyce CM. Discrimination against purine-pyrimidine mispairs in the polymerase active site of DNA polymerase I: a structural explanation. Proc Natl Acad Sci USA 2002; 99: 1194-1199.
71. Suzuki M, Yoshida S, Adman ET, Blank A, Loeb LA. Thermus aquaticus DNA polymerase I mutants with altered fidelity. Interacting mutations in the O-helix. J Biol Chem 2000; 275: 32728-32735.
72. Sjölander K, Karplus K, Brown M, Hughey R, Krogh A, Mian IS, Haussler D. Dirichlet mixtures: a method for improved detection of weak but significant protein sequence homology. Comput Appl Biosci 1996; 12: 327-345.
73. Sunyaev S, Ramensky V, Koch I, Lathe W, III, Kondrashov AS, Bork P. Prediction of deleterious human alleles. Hum Mol Genet 2001; 10: 591-597.
74. Sunyaev S, Ramensky V, Bork P. Towards a structural basis of human non-synonymous single nucleotide polymorphisms. Trends Genet 2000; 16: 198-200.
75. Sunyaev S, Hanke J, Aydin A, Wirkner U, Zastrow I, Reich J, Bork P. Prediction of nonsynonymous single nucleotide polymorphisms in human disease-associated genes. J Mol Med 1999; 77: 754-760.
76. Henrick K, Thornton JM. PQS: a protein quaternary structure file server. Trends Biochem. Sci 1998; 23: 358-361.
77. Fredman D, Siegfried M, Yuan YP, Bork P, Lehvaslaiho H, Brookes AJ. HGVbase: a human sequence variation database emphasizing data quality and a broad spectrum of data sources. Nucleic Acids Res 2002; 30: 387-391.
78. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22: 4673-4680.
79. Canutescu AA, Shelenkov AA, Dunbrack RL, Jr. A graph-theory algorithm for rapid protein side-chain prediction. Protein Sci 2003; 12: 2001-2014.
80. Gasteiger E, Jung E, Bairoch A. SWISS-PROT: connecting biomolecular knowledge via a protein database. Curr Issues Mol Biol 2001; 3: 47-55.
81. Baldi P, Chauvin Y, Hunkapiller T, McClure MA, Hidden Markov models of biological primary sequence information. Proc Natl Acad Sci USA 1994; 91: 1059-1063.
82. Henikoff S, Henikoff JG. Amino acid substitution matrices from protein blocks. Proc Natl Acad Sci USA 1992; 89: 10915-10919.
83. Chandonia JM, Hon G, Walker NS, Lo Conte L, Koehl P, Levitt M, Brenner SE. The ASTRAL Compendium in 2004. Nucleic Acids Res 2004; 32: D189-D192.
84. Meier M, Oliveriusova J, Kraus JP, Burkhard P. Structural insights into mutations of cystathionine beta-synthase. Biochim. Biophys Acta 2003; 1647: 206-213.
85. Stenberg KA, Vihinen M. Crystal structure of a 1.6-hexanediol bound tetrameric form of Escherichia coli lac-repressor refined to 2.1 A resolution. Proteins 2009; 75: 748-759.
86. Bateman A. The structure of a domain common to archaebacteria and the homocystinuria disease protein. Trends Biochem Sci 1997; 22: 12-13.
87. Xu Q, Canutescu A, Obradovic Z, Dunbrack RL, Jr. ProtBuD: a database of biological unit structures of protein families and superfamilies. Bioinformatics 2006; 22: 2876-2882.
88. Xu Q, Canutescu AA, Wang G, Shapovalov M, Obradovic Z, Dunbrack RL, Jr. Statistical analysis of interface similarity in crystals of homologous proteins. J Mol Biol 2008; 381: 487-507.
89. MacArthur MW, Thornton JM. Influence of proline residues on protein conformation, J Mol Biol 1991; 218: 397-412.
90. Kryshtafovych A, Venclovas C, Fidelis K, Moult J. Progress over the first decade of CASP experiments. Proteins: Struct Funct Genet 2005; 61 (Suppl 7): 225-236.
91. Janin J, Henrick K, Moult J, Eyck LT, Sternberg MJ, Vajda S, Vakser I, Wodak SJ. CAPRI: a critical assessment of PRedicted interactions. Proteins: Struct Funct Genet 2003; 52: 2-9.
92. Krivov GG, Shapovalov MV, Dunbrack RL, Jr. Improved prediction of protein side-chain conformations with SCWRL4. Proteins 2009; 77: 778-795.