Multifactorial likelihood assessment of BRCA1 and BRCA2 missense variants confirms that BRCA1:c.122A>G(p.His41Arg) is a pathogenic mutation

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Whiley, Phillip J ^a,b   Parsons, Michael T ^a   Leary, Jennifer ^c   Tucker, Kathy ^d   Warwick, Linda ^e   Dopita, Belinda ^e   Thorne, Heather ^f   Lakhani, Sunil R ^g   Goldgar, David E ^h   Brown, Melissa A ^b   Spurdle, Amanda B ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

^d PRINCE OF WALES HOSPITAL   (Australia)

^e CANBERRA HOSPITAL   (Australia)

^f PETER MACCALLUM CANCER CENTRE   (Australia)

^g UNIVERSITY OF QUEENSLAND   (Australia)

^h UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; MESSENGER RNA; UBIQUITIN PROTEIN LIGASE; BRCA1 PROTEIN; BRCA2 PROTEIN;

ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; EXON; HUMAN; MISSENSE MUTATION; MULTIFACTORIAL LIKELIHOOD ANALYSIS; NUCLEOTIDE SEQUENCE; PREDICTION; RNA SPLICING; STATISTICAL ANALYSIS; TUMOR SUPPRESSOR GENE; ALTERNATIVE RNA SPLICING; BIOLOGY; GENE DELETION; GENETIC PREDISPOSITION; GENETICS; METABOLISM; MULTIFACTORIAL INHERITANCE; REPRODUCIBILITY; STATISTICAL MODEL;

ALTERNATIVE SPLICING; BRCA1 PROTEIN; BRCA2 PROTEIN; COMPUTATIONAL BIOLOGY; EXONS; GENETIC PREDISPOSITION TO DISEASE; HUMANS; LIKELIHOOD FUNCTIONS; MULTIFACTORIAL INHERITANCE; MUTATION, MISSENSE; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; SEQUENCE DELETION;

EID: 84900301089     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086836     Document Type: Article

References (49)

1. Goldgar DE, Easton DF, Byrnes GB, Spurdle AB, Iversen ES, et al. (2008) Genetic evidence and integration of various data sources for classifying uncertain variants into a single model. Hum Mutat 29: 1265-1272.
2. Spurdle AB (2010) Clinical relevance of rare germline sequence variants in cancer genes: evolution and application of classification models. Curr Opin Genet Dev 20: 315-323.
3. Plon SE, Eccles DM, Easton D, Foulkes WD, Genuardi M, et al. (2008) Sequence variant classification and reporting: recommendations for improving the interpretation of cancer susceptibility genetic test results. Hum Mutat 29: 1282-1291.
4. Raponi M, Douglas AG, Tammaro C, Wilson DI, Baralle D (2012) Evolutionary constraint helps unmask a splicing regulatory region in BRCA1 exon 11. PLoS One 7: e37255.
5. Thery JC, Krieger S, Gaildrat P, Revillion F, Buisine MP, et al. (2011) Contribution of bioinformatics predictions and functional splicing assays to the interpretation of unclassified variants of the BRCA genes. Eur J Hum Genet 19: 1052-1058.
6. Vallee MP, Francy TC, Judkins MK, Babikyan D, Lesueur F, et al. (2012) Classification of missense substitutions in the BRCA genes: a database dedicated to Ex-UVs. Hum Mutat 33: 22-28.
7. Domchek SM, Tang J, Stopfer J, Lilli DR, Hamel N, et al. (2013) Biallelic deleterious BRCA1 mutations in a woman with early-onset ovarian cancer. Cancer Discov 3: 399-405.
8. Goldgar DE, Easton DF, Deffenbaugh AM, Monteiro ANA, Tavtigian SV, et al. (2004) Integrated evaluation of DNA sequence variants of unknown clinical significance: application to BRCA1 and BRCA2. American Journal Of Human Genetics 75: 535-544. (Pubitemid 39244769)
9. Lee MS, Green R, Marsillac SM, Coquelle N, Williams RS, et al. (2010) Comprehensive analysis of missense variations in the BRCT domain of BRCA1 by structural and functional assays. Cancer Res 70: 4880-4890.
10. Millot GA, Carvalho MA, Caputo SM, Vreeswijk MP, Brown MA, et al. (2012) A guide for functional analysis of BRCA1 variants of uncertain significance. Hum Mutat 33: 1526-1537.
11. Guidugli L, Pankratz VS, Singh N, Thompson J, Erding CA, et al. (2013) A Classification Model for BRCA2 DNA Binding Domain Missense Variants Based on Homology-Directed Repair Activity. Cancer Res 73: 265-275.
12. Mann GJ, Thorne H, Balleine RL, Butow PN, Clarke CL, et al. (2006) Analysis of cancer risk and BRCA1 and BRCA2 mutation prevalence in the kConFab familial breast cancer resource. Breast Cancer Res 8: R12.
13. Cartegni L, Wang J, Zhu Z, Zhang MQ, Krainer AR (2003) ESEfinder: A web resource to identify exonic splicing enhancers. Nucleic Acids Res 31: 3568-3571. (Pubitemid 37442199)
14. Desmet FO, Hamroun D, Lalande M, Collod-Beroud G, Claustres M, et al. (2009) Human Splicing Finder: an online bioinformatics tool to predict splicing signals. Nucleic Acids Res 37: e67.
15. Yeo G, Burge CB (2004) Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J Comput Biol 11: 377-394. (Pubitemid 38901668)
16. Reese MG, Eeckman FH, Kulp D, Haussler D (1997) Improved splice site detection in Genie. J Comput Biol 4: 311-323. (Pubitemid 27355870)
17. Bateman JF, Freddi S, Lamande SR, Byers P, Nasioulas S, et al. (1999) Reliable and sensitive detection of premature termination mutations using a protein truncation test designed to overcome problems of nonsense-mediated mRNA instability. Hum Mutat 13: 311-317. (Pubitemid 29307076)
18. Walker LC, Whiley PJ, Houdayer C, Hansen TV, Vega A, et al. (2013) Evaluation of a 5-tier scheme proposed for classification of sequence variants using bioinformatic and splicing assay data: inter-reviewer variability and promotion of minimum reporting guidelines. Hum Mutat 34: 1424-1431.
19. Lakhani SR, Gusterson BA, Jacquemier J, Sloane JP, Anderson TJ, et al. (2000) The pathology of familial breast cancer: histological features of cancers in families not attributable to mutations in BRCA1 or BRCA2. Clin Cancer Res 6: 782-789. (Pubitemid 30159330)
20. Walker LC, Whiley PJ, Couch FJ, Farrugia DJ, Healey S, et al. (2010) Detection of splicing aberrations caused by BRCA1 and BRCA2 sequence variants encoding missense substitutions: implications for prediction of pathogenicity. Hum Mutat 31: E1484-1505.
21. Chenevix-Trench G, Healey S, Lakhani S, Waring P, Cummings M, et al. (2006) Genetic and histopathologic evaluation of BRCA1 and BRCA2 DNA sequence variants of unknown clinical significance. Cancer Res 66: 2019-2027.
22. Spurdle AB, Lakhani SR, Healey S, Parry S, Da Silva LM, et al. (2008) Clinical classification of BRCA1 and BRCA2 DNA sequence variants: the value of cytokeratin profiles and evolutionary analysis-a report from the kConFab Investigators. J Clin Oncol 26: 1657-1663.
23. Goldgar DE, Easton DF, Deffenbaugh AM, Monteiro AN, Tavtigian SV, et al. (2004) Integrated evaluation of DNA sequence variants of unknown clinical significance: application to BRCA1 and BRCA2. Am J Hum Genet 75: 535-544. (Pubitemid 39244769)
24. Easton DF, Deffenbaugh AM, Pruss D, Frye C, Wenstrup RJ, et al. (2007) A systematic genetic assessment of 1,433 sequence variants of unknown clinical significance in the BRCA1 and BRCA2 breast cancer-predisposition genes. Am J Hum Genet 81: 873-883. (Pubitemid 47580242)
25. Domchek SM, Tang JB, Stopfer J, Lilli DR, Hamel N, et al. (2012) Biallelic Deleterious BRCA1 Mutations in a Woman with Early-Onset Ovarian Cancer. Cancer Discov.
26. Cartegni L, Chew SL, Krainer AR (2002) Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nature Reviews Genetics 3: 285-298. (Pubitemid 34279797)
27. Orban TI, Olah E (2003) Emerging roles of BRCA1 alternative splicing. Mol Pathol 56: 191-197. (Pubitemid 36981151)
28. Whiley P, de la Hoya M, Thomassen M, Becker A, Brandao R, et al. (2013) Comparison of mRNA Splicing Assay Protocols across Multiple Laboratories: Recommendations for Best Practice in Standardized Clinical Testing. Clin Chem.
29. Ozcelik H, Nedelcu R, Chan VW, Shi XH, Murphy J, et al. (1999) Mutation in the coding region of the BRCA1 gene leads to aberrant splicing of the transcript. Hum Mutat 14: 540-541.
30. Yang Y, Swaminathan S, Martin BK, Sharan SK (2003) Aberrant splicing induced by missense mutations in BRCA1: clues from a humanized mouse model. Human Molecular Genetics 12: 2121-2131. (Pubitemid 37098984)
31. Hu YF, Li R (2002) JunB potentiates function of BRCA1 activation domain 1 (AD1) through a coiled-coil-mediated interaction. Genes Dev 16: 1509-1517.
32. Sum EY, Peng B, Yu X, Chen J, Byrne J, et al. (2002) The LIM domain protein LMO4 interacts with the cofactor CtIP and the tumor suppressor BRCA1 and inhibits BRCA1 activity. J Biol Chem 277: 7849-7856. (Pubitemid 34968233)
33. Yarden RI, Brody LC (1999) BRCA1 interacts with components of the histone deacetylase complex. Proc Natl Acad Sci U S A 96: 4983-4988. (Pubitemid 29214522)
34. Hu YF, Miyake T, Ye Q, Li R (2000) Characterization of a novel transactivation domain of BRCA1 that functions in concert with the BRCA1 Cterminal (BRCT) domain. J Biol Chem 275: 40910-40915. (Pubitemid 32054913)
35. Phelan CM, Dapic V, Tice B, Favis R, Kwan E, et al. (2005) Classification of BRCA1 missense variants of unknown clinical significance. J Med Genet 42: 138-146. (Pubitemid 40204368)
36. Sevcik J, Falk M, Kleiblova P, Lhota F, Stefancikova L, et al. (2012) The BRCA1 alternative splicing variant Delta14-15 with an in-frame deletion of part of the regulatory serine-containing domain (SCD) impairs the DNA repair capacity in MCF-7 cells. Cell Signal 24: 1023-1030.
37. Spurdle AB, Couch FJ, Hogervorst FB, Radice P, Sinilnikova OM (2008) Prediction and assessment of splicing alterations: implications for clinical testing. Hum Mutat 29: 1304-1313.
38. Gaildrat P, Krieger S, Di Giacomo D, Abdat J, Revillion F, et al. (2012) Multiple sequence variants of BRCA2 exon 7 alter splicing regulation. J Med Genet 49: 609-617.
39. Brzovic PS, Rajagopal P, Hoyt DW, King MC, Klevit RE (2001) Structure of a BRCA1-BARD1 heterodimeric RING-RING complex. Nat Struct Biol 8: 833-837. (Pubitemid 32923599)
40. Chen A, Kleiman FE, Manley JL, Ouchi T, Pan ZQ (2002) Autoubiquitination of the BRCA1*BARD1 RING ubiquitin ligase. J Biol Chem 277: 22085-22092. (Pubitemid 34952363)
41. Xia Y, Pao GM, Chen HW, Verma IM, Hunter T (2003) Enhancement of BRCA1 E3 ubiquitin ligase activity through direct interaction with the BARD1 protein. J Biol Chem 278: 5255-5263. (Pubitemid 36801039)
42. Ransburgh DJ, Chiba N, Ishioka C, Toland AE, Parvin JD (2010) Identification of breast tumor mutations in BRCA1 that abolish its function in homologous DNA recombination. Cancer Res 70: 988-995.
43. Morris JR, Pangon L, Boutell C, Katagiri T, Keep NH, et al. (2006) Genetic analysis of BRCA1 ubiquitin ligase activity and its relationship to breast cancer susceptibility. Hum Mol Genet 15: 599-606. (Pubitemid 43205424)
44. Bouwman P, van der Gulden H, van der Heijden I, Drost R, Klijn CN, et al. (2013) A high-throughput functional complementation assay for classification of BRCA1 missense variants. Cancer Discov.
45. Shakya R, Reid LJ, Reczek CR, Cole F, Egli D, et al. (2011) BRCA1 tumor suppression depends on BRCT phosphoprotein binding, but not its E3 ligase activity. Science 334: 525-528.
46. Sarkar M, Magliery TJ (2008) Re-engineering a split-GFP reassembly screen to examine RING-domain interactions between BARD1 and BRCA1 mutants observed in cancer patients. Mol Biosyst 4: 599-605. (Pubitemid 351706303)
47. Sweet K, Senter L, Pilarski R, Wei L, Toland AE (2010) Characterization of BRCA1 ring finger variants of uncertain significance. Breast Cancer Res Treat 119: 737-743.
48. Ruffner H, Joazeiro CA, Hemmati D, Hunter T, Verma IM (2001) Cancer-predisposing mutations within the RING domain of BRCA1: loss of ubiquitin protein ligase activity and protection from radiation hypersensitivity. Proc Natl Acad Sci U S A 98: 5134-5139. (Pubitemid 32397095)
49. Chang S, Biswas K, Martin BK, Stauffer S, Sharan SK (2009) Expression of human BRCA1 variants in mouse ES cells allows functional analysis of BRCA1 mutations. J Clin Invest 119: 3160-3171.