Performance of In Silico Tools for the Evaluation of UGT1A1 Missense Variants

Human Mutation

Volumn 36, Issue 12, 2015, Pages 1215-1225

  Rodrigues, Carina ^a,b   Santos Silva, Alice ^a   Costa, Elísio ^a   Bronze da Rocha, Elsa ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b INSTITUTO POLITÉCNICO DE BRAGANÇA   (Portugal)

Author keywords

Bioinformatics; Genotype; NsSNPs; Phenotype; Protein function; UGT1A1

Indexed keywords

MESSENGER RNA PRECURSOR; GLUCURONOSYLTRANSFERASE; UGT1A1 ENZYME;

ALGORITHM; ARTICLE; BIOINFORMATICS; COMPUTER MODEL; COMPUTER PROGRAM; CORRELATION COEFFICIENT; GENE; GENETIC VARIABILITY; IN VITRO STUDY; IN VIVO STUDY; MACHINE LEARNING; MISSENSE MUTATION; MUTPRED; PATHOGENICITY; PHENOTYPE; POLYPHEN 2; PREDICTION OF PATHOLOGICAL MUTATIONS ON PROTEIN; PRIORITY JOURNAL; PROTEIN FUNCTION; SENSITIVITY ANALYSIS; SENSITIVITY AND SPECIFICITY; SINGLE NUCLEOTIDE POLYMORPHISM; SORTING INTOLERANT FROM TOLERANT; URIDINE DIPHOSPHATE GLUCURONOSYLTRANSFERASE 1A1 GENE; AMINO ACID SUBSTITUTION; BIOLOGY; GENETICS; HUMAN; MOLECULAR EVOLUTION; NUCLEIC ACID DATABASE; PROCEDURES; WEB BROWSER;

AMINO ACID SUBSTITUTION; COMPUTATIONAL BIOLOGY; DATABASES, NUCLEIC ACID; EVOLUTION, MOLECULAR; GLUCURONOSYLTRANSFERASE; HUMANS; MUTATION, MISSENSE; POLYMORPHISM, SINGLE NUCLEOTIDE; SOFTWARE; WEB BROWSER;

EID: 84946554973     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.22903     Document Type: Article

References (65)

1. Acharya V, Nagarajaram HÁ. 2012. Hansa: an automated method for discriminating disease and neutral human nsSNPs. Hum Mutat 33:332-337.
2. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR. 2010. A method and server for predicting damaging missense mutations. Nat Methods 7:248-249.
3. Aono S, Adachi Y, Uyama E, Yamada Y, Keino H, Nanno T, Koiwai O, Sato H. 1995. Analysis of genes for bilirubin UDP-glucuronosyltransferase in Gilbert's syndrome. Lancet 345:958-959.
4. Baldi P, Brunak S, Chauvin Y, Andersen CA, Nielsen H. 2000. Assessing the accuracy of prediction algorithms for classification: an overview. Bioinformatics 16:412-424.
5. Bosma PJ, Chowdhury JR, Bakker C, Gantla S, de Boer A, Oostra BA, Lindhout D, Tytgat GN, Jansen PL, Oude Elferink RP, Chowdhury NR. 1995. The genetic basis of the reduced expression of bilirubin UDP-glucuronosyltransferase 1 in Gilbert's syndrome. N Engl J Med 333:1171-1175.
6. Bromberg Y, Rost B. 2007. SNAP: predict effect of non-synonymous polymorphisms on function. Nucleic Acid Res 35:3823-3835.
7. Bromberg Y, Yachdav G, Rost B. 2008. SNAP predicts effect of mutations on protein function. Bioinformatics 24:2397-2398.
8. Calabrese R, Capriotti E, Fariselli P, Martelli PL, Casadio R. 2009. Functional annotations improve the predictive score of human disease-related mutations in proteins. Hum Mutat 30:1237-1244.
9. Capriotti E, Altman RB, Bromberg Y. 2013. Collective judgment predicts disease-associated single nucleotide variants. BMC Genomics 14 Suppl 3:S2.
10. 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.
11. Ciotti M, Chen F, Rubaltelli FF, Owens IS. 1998. Coding defect and a TATA box mutation at the bilirubin UDP-glucuronosyltransferase gene cause Crigler-Najjar type I disease. Biochim Biophys Acta 1407:40-50.
12. Costa E. 2006. Hematologically important mutations: bilirubin UDP-glucuronosyltransferase gene mutations in Gilbert and Crigler-Najjar syndromes. Blood Cells Mol Dis 36:77-80.
13. Costa E, Vieira E, Martins M, Saraiva J, Cancela E, Costa M, Bauerle R, Freitas T, Carvalho JR, Santos-Silva A, Barbot J, Dos Santos R. 2006. Analysis of the UDP-glucuronosyltransferase gene in Portuguese patients with a clinical diagnosis of Gilbert and Crigler-Najjar syndromes. Blood Cells Mol Dis 36:91-97.
14. De Baets G, Van Durme J, Reumers J, Maurer-Stroh S, Vanhee P, Dopazo J, Schymkowitz J, Rousseau F. 2012. SNPeffect 4.0: on-line prediction of molecular and structural effects of protein-coding variants. Nucleic Acids Res 40:D935-D939.
15. Deiss A. 1999. Destruction of erythrocytes. In: Wintrobe's clinical haematology. Vol. 10. Baltimore, MD: Lippincott Williams & Wilkins. p 267-299.
16. Desmet FO, Hamroun D, Lalande M, Collod-Béroud G, Claustres M, Béroud C. 2009. Human splicing finder: an online bioinformatics tool to predict splicing signals. Nucleic Acids Res 37:e67.
17. Di YM, Chan E, Wei MQ, Liu JP, Zhou SF. 2009. Prediction of deleterious non-synonymous single-nucleotide polymorphisms of human uridine diphosphate glucuronosyltransferase genes. AAPS J 11:469-480.
18. Farheen S, Sengupta S, Santra A, Pal S, Dhali GK, Chakravorty M, Majumder PP, Chowdhury A. 2006. Gilbert's syndrome: high frequency of the (TA)7 TAA allele in India and its interaction with a novel CAT insertion in promoter of the gene for bilirubin UDP-glucuronosyltransferase 1 gene. World J Gastroenterol 12:2269-2275.
19. Ferrer-Costa C, Gelpi JL, Zamakola L, Parraga I, de la Cruz X, Orozco M. 2005. PMUT: a web-based tool for the annotation of pathological mutations on proteins. Bioinformatics 21:3176-3178.
20. Ferrer-Costa C, Orozco M, de la Cruz X. 2004. Sequence-based prediction of pathological mutations. Proteins 57:811-819.
21. Galehdari H, Saki N, Mohammadi-Asl J, Rahim F. 2013. Meta-analysis diagnostic accuracy of SNP-based pathogenicity detection tools: a case of UTG1A1 gene mutations. Int J Mol Epidemiol Genet 4:774-785.
22. Garcia-Blanco MA, Baraniak AP, Lasda EL. 2004. Alternative splicing in disease and therapy. Nat Biotechnol 22:535-546.
23. Gonzalez-Perez A, Lopez-Bigas N. 2011. Improving the assessment of the outcome of nonsynonymous SNVs with a consensus deleteriousness score, Condel. Am J Hum Genet 88:440-449.
24. Hicks S, Plon SE, Kimmel M. 2013. Statistical analysis of missense mutation classifiers. Hum Mutat 34:405-406.
25. Hicks S, Wheeler DA, Plon SE, Kimmel M. 2011. Prediction of missense mutation functionality depends on both the algorithm and sequence alignment employed. Hum Mutat 32:661-668.
26. Hiltemann S, Mei H, deHollander M., Palli I, Spek P, Guido J, Andrew S. 2014. CGtag: complete genomics toolkit and annotation in a cloud-based Galaxy. Gigascience 3:1-6.
27. Huang CS, Luo GA, Huang ML, Yu SC, Yang SS. 2000. Variations of the bilirubin uridine-diphosphoglucuronosyl transferase 1A1 gene in healthy Taiwanese. Pharmacogenetics 10:539-544.
28. Johnson MM, Houck J, Chen C. 2005. Screening for Deleterious nonsynonymous single-nucleotide polymorphisms in genes involved in steroid hormone metabolism and response. Cancer Epidemiol Biomarkers Prev 14:1326-1329.
29. Jordan DM, Ramensky VE, Sunyaev SR. 2010. Human allelic variation: perspective from protein function, structure, and evolution. Curr Opin Struct Biol 20:342-350.
30. Kaniwa N, Kurose K, Jinno H, Tanaka-Kagawa T, Saito Y, Saeki M, Sawada J, Tohkin M, Hasegawa R. 2005. Racial variability in haplotype frequencies of UGT1A1 and glucuronidation activity of a novel single nucleotide polymorphism 686C>T (P229L) found in an African-American. Drug Metab Dispos 33:458-465.
31. Karchin R, Diekhans M, Kelly L, Thomas DJ, Pieper U, Eswar N, Haussler D, Sali A. 2005. LS-SNP: large-scale annotation of coding non-synonymous SNPs based on multiple information sources. Bioinformatics 21:2814-2820.
32. Katoh K, Standley DM. 2013. MAFFT Multiple Sequence Alignment Software Version 7: improvements in performance and usability. Mol Biol Evol 30:772-780.
33. 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.
34. Labrune P, Myara A, Chalas J, Le Bihan B, Capel L, Francoual J. 2002. Association of a homozygous (TA)8 promoter polymorphism and a N400D mutation of UGT1A1 in a child with Crigler-Najjar type II syndrome. Hum Mutat 20:399-401.
35. Labrune P, Myara A, Hadchouel M, Ronchi F, Bernard O, Trivin F, Chowdhury NR, Chowdhury JR, Munnich A, Odievre M. 1994. Genetic heterogeneity of Crigler-Najjar syndrome type I: a study of 14 cases. Hum Genet 94:693-697.
36. Lévesque E, Girard H, Journault K, Lépine J, Guillemette C. 2007. Regulation of the UGT1A1 bilirubin-conjugating pathway: role of a new splicing event at the UGT1A locus. Hepatology 45:128-138.
37. Li B, Krishnan VG, Mort ME, Xin F, Kamati KK, Cooper DN, Mooney SD, Radivojac P. 2009. Automated inference of molecular mechanisms of disease from amino acid substitutions. Bioinformatics 25:2744-2750.
38. Li C, Wu Q. 2007. Adaptive evolution of multiple-variable exons and structural diversity of drug-metabolizing enzymes. BMC Evol Biol 7:69-88.
39. Lopez-Bigas N, Audit B, Ouzounis C, Parra G, Guigo R. 2005. Are splicing mutations the most frequent cause of hereditary disease? FEBS Lett 579:1900-1903.
40. Lynch M, Katju V. 2004. The altered evolutionary trajectories of gene duplicates. Trends Genet 20:544-549.
41. Mackenzie PI. 1986. Rat liver UDP-glucuronosyltransferase. Sequence and expression of a cDNA encoding a phenobarbital-inducible form. J Biol Chem 261:6119-6125.
42. Matthews BW. 1975. Comparison of the predicted and observed secondary structure of T4 phage lysozyme. Biochim Biophys Acta 405:442-451.
43. Mi H, Muruganujan A, Casagrande JT, Thomas PD. 2013. Large-scale gene function analysis with the PANTHER classification system. Nat Protoc 8:1551-1566.
44. Ng PC, Henikoff S. 2006. Predicting the effects of amino acid substitutions on protein function. Annu Rev Genomics Hum Genet 7:61-80.
45. Reumers J, Maurer-Stroh S, Schymkowitz J, Rousseau F. 2006. SNPeffect v2.0: a new step in investigating the molecular phenotypic effects of human non-synonymous SNPs. Bioinformatics 22:2183-2185.
46. Reva B, Antipin Y, Sander C. 2011. Predicting the functional impact of protein mutations: application to cancer genomics. Nucleic Acids Res 39:e118.
47. Rodrigues C, Vieira E, Santos R, de Carvalho J, Santos-Silva A, Costa E, Bronze-da-Rocha E. 2012. Impact of UGT1A1 gene variants on total bilirubin levels in Gilbert syndrome patients and in healthy subjects. Blood Cells Mol Dis 48:166-172.
48. Sai K, Saeki M, Saito Y, Ozawa S, Katori N, Jinno H, Hasegawa R, Kaniwa N, Sawada J, Komamura K, Ueno K, Kamakura S, et al. 2004. UGT1A1 haplotypes associated with reduced glucuronidation and increased serum bilirubin in irinotecan-administered Japanese patients with cancer. Clin Pharmacol Ther 75:501-515.
49. Seppen J, Bosma PJ, Goldhoorn BG, Bakker CT, Chowdhury JR, Chowdhury NR, Jansen PL, Oude Elferink RP. 1994. Discrimination between Crigler-Najjar type I and II by expression of mutant bilirubin uridine diphosphate-glucuronosyltransferase. J Clin Invest 94:2385-2391.
50. Shihab HA, Gough J, Cooper DN, Stenson PD, Barker GL, Edwards KJ, Day IN, Gaunt TR. 2013. Predicting the functional, molecular, and phenotypic consequences of amino acid substitutions using hidden Markov models. Hum Mutat 34:57-65.
51. Shu Y, Leabman MK, Feng B, Mangravite LM, Huang CC, Stryke D, Kawamoto M, Johns SJ, DeYoung J, Carlson E, Ferrin TE, Herskowitz I, Giacomini KM; Pharmacogenetics Of Membrane Transporters Investigators. 2003. Evolutionary conservation predicts function of variants of the human organic cation transporter, OCT1. Proc Natl Acad Sci USA 100:5902-5907.
52. Sim NL, Kumar P, Hu J, Henikoff S, Schneider G, Ng PC. 2012. SIFT web server: predicting effects of amino acid substitutions on proteins. Nucleic Acids Res 40 (Web Server issue):W452-W457.
53. Sneitz N, Bakker CT, de Knegt RJ, Halley DJ, Finel M, Bosma PJ. 2010. Crigler-Najjar syndrome in The Netherlands: identification of four novel UGT1A1 alleles, genotype-phenotype correlation, and functional analysis of 10 missense mutants. Hum Mutat 31:52-59.
54. Sterne-Weiler T, Howard J, Mort M, Cooper DN, Sanford JR: 2011. Loss of exon identity is a common mechanism of human inherited disease. Genome Res 21:1563-1571.
55. Stone EA, Sidow A. 2005. Physicochemical constraint violation by missense substitutions mediates impairment of protein function and disease severity. Genome Res 15:978-986.
56. Strassburg CP, Lankisch TO, Manns MP, Ehmer U. 2008. Family 1 uridine-5'-diphosphate glucuronosyltransferases (UGT1A): from Gilbert's syndrome to genetic organization and variability. Arch Toxicol 82:415-433.
57. Sutomo R, Laosombat V, Sadewa AH, Yokoyama N, Nakamura H, Matsuo M, Nishio H. 2002. Novel missense mutation of the UGT1A1 gene in Thai siblings with Gilbert's syndrome. Pediatr Int 44:427-432.
58. Tavtigian SV, Deffenbaugh AM, Yin L, Judkins T, Scholl T, Samollow PB, de Silva D, Zharkikh A, Thomas A. 2006. Comprehensive statistical study of 452 BRCA1 missense substitutions with classification of eight recurrent substitutions as neutral. J Med Genet 43:295-305.
59. Thomas PD, Kejariwal A, Campbell MJ, Mi H, Diemer K, Guo N, Ladunga I, Ulitsky-Lazareva B, Muruganujan A, Rabkin S, Vandergriff JA, Doremieux O. 2003. PANTHER: a browsable database of gene products organized by biological function, using curated protein family and subfamily classification. Nucleic Acids Res 31:334-341.
60. Thusberg J, Olatubosun A, Vihinen M. 2011. Performance of mutation pathogenicity prediction methods on missense variants. Hum Mutat 32:358-368.
61. Vihinen M. 2012. How to evaluate performance of prediction methods? Measures and their interpretation in variation effect analysis. BMC Genomics 13 Suppl 4:S2.
62. Vihinen M. 2013. Guidelines for reporting and using prediction tools for genetic variation analysis. Hum Mutat 34:275-282.
63. Wang Z, Moult J. 2001. SNPs, protein structure, and disease. Hum Mutat 17:263-270.
64. Wong KC, Zhang Z. 2014. SNPdryad: predicting deleterious non-synonymous human SNPs using only orthologous protein sequences. Bioinformatics 30:112-119.
65. Yusoff S, Van Rostenberghe H, Yusoff NM, Talib NA, Ramli N, Ismail NZ, Ismail WP, Matsuo M, Nishio H. 2006. Frequencies of A(TA)7TAA, G71R, and G493R mutations of the UGT1A1 gene in the Malaysian population. Biol Neonate 89:171-176.