Literature DB >> 24212087

Comparison of mRNA splicing assay protocols across multiple laboratories: recommendations for best practice in standardized clinical testing.

Phillip J Whiley1, Miguel de la Hoya, Mads Thomassen, Alexandra Becker, Rita Brandão, Inge Sokilde Pedersen, Marco Montagna, Mireia Menéndez, Francisco Quiles, Sara Gutiérrez-Enríquez, Kim De Leeneer, Anna Tenés, Gemma Montalban, Demis Tserpelis, Toshio Yoshimatsu, Carole Tirapo, Michela Raponi, Trinidad Caldes, Ana Blanco, Marta Santamariña, Lucia Guidugli, Gorka Ruiz de Garibay, Ming Wong, Mariella Tancredi, Laura Fachal, Yuan Chun Ding, Torben Kruse, Vanessa Lattimore, Ava Kwong, Tsun Leung Chan, Mara Colombo, Giovanni De Vecchi, Maria Caligo, Diana Baralle, Conxi Lázaro, Fergus Couch, Paolo Radice, Melissa C Southey, Susan Neuhausen, Claude Houdayer, Jim Fackenthal, Thomas Van Overeem Hansen, Ana Vega, Orland Diez, Rien Blok, Kathleen Claes, Barbara Wappenschmidt, Logan Walker, Amanda B Spurdle, Melissa A Brown.   

Abstract

BACKGROUND: Accurate evaluation of unclassified sequence variants in cancer predisposition genes is essential for clinical management and depends on a multifactorial analysis of clinical, genetic, pathologic, and bioinformatic variables and assays of transcript length and abundance. The integrity of assay data in turn relies on appropriate assay design, interpretation, and reporting.
METHODS: We conducted a multicenter investigation to compare mRNA splicing assay protocols used by members of the ENIGMA (Evidence-Based Network for the Interpretation of Germline Mutant Alleles) consortium. We compared similarities and differences in results derived from analysis of a panel of breast cancer 1, early onset (BRCA1) and breast cancer 2, early onset (BRCA2) gene variants known to alter splicing (BRCA1: c.135-1G>T, c.591C>T, c.594-2A>C, c.671-2A>G, and c.5467+5G>C and BRCA2: c.426-12_8delGTTTT, c.7988A>T, c.8632+1G>A, and c.9501+3A>T). Differences in protocols were then assessed to determine which elements were critical in reliable assay design.
RESULTS: PCR primer design strategies, PCR conditions, and product detection methods, combined with a prior knowledge of expected alternative transcripts, were the key factors for accurate splicing assay results. For example, because of the position of primers and PCR extension times, several isoforms associated with BRCA1, c.594-2A>C and c.671-2A>G, were not detected by many sites. Variation was most evident for the detection of low-abundance transcripts (e.g., BRCA2 c.8632+1G>A Δ19,20 and BRCA1 c.135-1G>T Δ5q and Δ3). Detection of low-abundance transcripts was sometimes addressed by using more analytically sensitive detection methods (e.g., BRCA2 c.426-12_8delGTTTT ins18bp).
CONCLUSIONS: We provide recommendations for best practice and raise key issues to consider when designing mRNA assays for evaluation of unclassified sequence variants.

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Year:  2013        PMID: 24212087      PMCID: PMC4351044          DOI: 10.1373/clinchem.2013.210658

Source DB:  PubMed          Journal:  Clin Chem        ISSN: 0009-9147            Impact factor:   8.327


  29 in total

1.  Functional assays for classification of BRCA2 variants of uncertain significance.

Authors:  Daniel J Farrugia; Mukesh K Agarwal; Vernon S Pankratz; Amie M Deffenbaugh; Dmitry Pruss; Cynthia Frye; Linda Wadum; Kiley Johnson; Jennifer Mentlick; Sean V Tavtigian; David E Goldgar; Fergus J Couch
Journal:  Cancer Res       Date:  2008-05-01       Impact factor: 12.701

2.  Evaluation of in silico splice tools for decision-making in molecular diagnosis.

Authors:  Claude Houdayer; Catherine Dehainault; Christophe Mattler; Dorothée Michaux; Virginie Caux-Moncoutier; Sabine Pagès-Berhouet; Catherine Dubois d'Enghien; Anthony Laugé; Laurent Castera; Marion Gauthier-Villars; Dominique Stoppa-Lyonnet
Journal:  Hum Mutat       Date:  2008-07       Impact factor: 4.878

3.  Reliable genotyping of samples with very low DNA quantities using PCR.

Authors:  P Taberlet; S Griffin; B Goossens; S Questiau; V Manceau; N Escaravage; L P Waits; J Bouvet
Journal:  Nucleic Acids Res       Date:  1996-08-15       Impact factor: 16.971

4.  Molecular characterization and cancer risk associated with BRCA1 and BRCA2 splice site variants identified in multiple-case breast cancer families.

Authors:  A A Tesoriero; E M Wong; M A Jenkins; J L Hopper; M A Brown; G Chenevix-Trench; A B Spurdle; M C Southey
Journal:  Hum Mutat       Date:  2005-11       Impact factor: 4.878

5.  Genetic, functional, and histopathological evaluation of two C-terminal BRCA1 missense variants.

Authors:  P K Lovelock; S Healey; W Au; E Y M Sum; A Tesoriero; E M Wong; S Hinson; R Brinkworth; A Bekessy; O Diez; L Izatt; E Solomon; M Jenkins; H Renard; J Hopper; P Waring; S V Tavtigian; D Goldgar; G J Lindeman; J E Visvader; F J Couch; B R Henderson; M Southey; G Chenevix-Trench; A B Spurdle; M A Brown
Journal:  J Med Genet       Date:  2005-05-27       Impact factor: 6.318

6.  Intronic alterations in BRCA1 and BRCA2: effect on mRNA splicing fidelity and expression.

Authors:  Xiaowei Chen; Tuyet-Trinh N Truong; JoEllen Weaver; Betsy A Bove; Kimberly Cattie; Brock A Armstrong; Mary B Daly; Andrew K Godwin
Journal:  Hum Mutat       Date:  2006-05       Impact factor: 4.878

7.  Screening BRCA1 and BRCA2 unclassified variants for splicing mutations using reverse transcription PCR on patient RNA and an ex vivo assay based on a splicing reporter minigene.

Authors:  C Bonnet; S Krieger; M Vezain; A Rousselin; I Tournier; A Martins; P Berthet; A Chevrier; C Dugast; V Layet; A Rossi; R Lidereau; T Frébourg; A Hardouin; M Tosi
Journal:  J Med Genet       Date:  2008-04-18       Impact factor: 6.318

8.  Differentiating pathogenic mutations from polymorphic alterations in the splice sites of BRCA1 and BRCA2.

Authors:  Kathleen Claes; Bruce Poppe; Eva Machackova; Ilse Coene; Lenka Foretova; Anne De Paepe; Ludwine Messiaen
Journal:  Genes Chromosomes Cancer       Date:  2003-07       Impact factor: 5.006

9.  Germline mutations of the BRCA1 gene in breast and ovarian cancer families provide evidence for a genotype-phenotype correlation.

Authors:  S A Gayther; W Warren; S Mazoyer; P A Russell; P A Harrington; M Chiano; S Seal; R Hamoudi; E J van Rensburg; A M Dunning; R Love; G Evans; D Easton; D Clayton; M R Stratton; B A Ponder
Journal:  Nat Genet       Date:  1995-12       Impact factor: 38.330

10.  Spectrum and characterisation of BRCA1 and BRCA2 deleterious mutations in high-risk Czech patients with breast and/or ovarian cancer.

Authors:  Eva Machackova; Lenka Foretova; Mirka Lukesova; Petra Vasickova; Marie Navratilova; Ilse Coene; Hana Pavlu; Veronika Kosinova; Jitka Kuklova; Kathleen Claes
Journal:  BMC Cancer       Date:  2008-05-20       Impact factor: 4.430

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  31 in total

1.  RNA analysis of cancer predisposing genes in formalin-fixed paraffin-embedded tissue determines aberrant splicing.

Authors:  Anne Ml Jansen; Heleen M van der Klift; Marieke Ae Roos; Jaap Dh van Eendenburg; Carli Mj Tops; Juul T Wijnen; Frederik J Hes; Hans Morreau; Tom van Wezel
Journal:  Eur J Hum Genet       Date:  2018-04-30       Impact factor: 4.246

2.  Full-length transcript amplification and sequencing as universal method to test mRNA integrity and biallelic expression in mismatch repair genes.

Authors:  Monika Morak; Kerstin Schaefer; Verena Steinke-Lange; Udo Koehler; Susanne Keinath; Trisari Massdorf; Brigitte Mauracher; Nils Rahner; Jessica Bailey; Christiane Kling; Tanja Haeusser; Andreas Laner; Elke Holinski-Feder
Journal:  Eur J Hum Genet       Date:  2019-07-22       Impact factor: 4.246

3.  Epigenetic changes in healthy human skeletal muscle following exercise- a systematic review.

Authors:  Macsue Jacques; Danielle Hiam; Jeffrey Craig; Romain Barrès; Nir Eynon; Sarah Voisin
Journal:  Epigenetics       Date:  2019-05-13       Impact factor: 4.528

4.  Implication of non-coding PAX6 mutations in aniridia.

Authors:  Julie Plaisancié; M Tarilonte; P Ramos; C Jeanton-Scaramouche; V Gaston; H Dollfus; D Aguilera; J Kaplan; L Fares-Taie; F Blanco-Kelly; C Villaverde; C Francannet; A Goldenberg; I Arroyo; J M Rozet; C Ayuso; N Chassaing; P Calvas; M Corton
Journal:  Hum Genet       Date:  2018-10-05       Impact factor: 4.132

Review 5.  Genetic predisposition to colorectal cancer: syndromes, genes, classification of genetic variants and implications for precision medicine.

Authors:  Laura Valle; Eduardo Vilar; Sean V Tavtigian; Elena M Stoffel
Journal:  J Pathol       Date:  2019-02-20       Impact factor: 7.996

6.  Characterization of three alternative transcripts of the BRCA1 gene in patients with breast cancer and a family history of breast and/or ovarian cancer who tested negative for pathogenic mutations.

Authors:  Gaetana Gambino; Mariella Tancredi; Elisabetta Falaschi; Paolo Aretini; Maria Adelaide Caligo
Journal:  Int J Mol Med       Date:  2015-02-16       Impact factor: 4.101

7.  BRCA1 Alternative splicing landscape in breast tissue samples.

Authors:  Atocha Romero; Francisco García-García; Irene López-Perolio; Gorka Ruiz de Garibay; José A García-Sáenz; Pilar Garre; Patricia Ayllón; Esperanza Benito; Joaquín Dopazo; Eduardo Díaz-Rubio; Trinidad Caldés; Miguel de la Hoya
Journal:  BMC Cancer       Date:  2015-04-03       Impact factor: 4.430

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

Authors:  Phillip J Whiley; Michael T Parsons; Jennifer Leary; Kathy Tucker; Linda Warwick; Belinda Dopita; Heather Thorne; Sunil R Lakhani; David E Goldgar; Melissa A Brown; Amanda B Spurdle
Journal:  PLoS One       Date:  2014-01-28       Impact factor: 3.240

9.  Combined genetic and splicing analysis of BRCA1 c.[594-2A>C; 641A>G] highlights the relevance of naturally occurring in-frame transcripts for developing disease gene variant classification algorithms.

Authors:  Miguel de la Hoya; Omar Soukarieh; Irene López-Perolio; Ana Vega; Logan C Walker; Yvette van Ierland; Diana Baralle; Marta Santamariña; Vanessa Lattimore; Juul Wijnen; Philip Whiley; Ana Blanco; Michela Raponi; Jan Hauke; Barbara Wappenschmidt; Alexandra Becker; Thomas V O Hansen; Raquel Behar; KConFaB Investigators; Diether Niederacher; Norbert Arnold; Bernd Dworniczak; Doris Steinemann; Ulrike Faust; Wendy Rubinstein; Peter J Hulick; Claude Houdayer; Sandrine M Caputo; Laurent Castera; Tina Pesaran; Elizabeth Chao; Carole Brewer; Melissa C Southey; Christi J van Asperen; Christian F Singer; Jan Sullivan; Nicola Poplawski; Phuong Mai; Julian Peto; Nichola Johnson; Barbara Burwinkel; Harald Surowy; Stig E Bojesen; Henrik Flyger; Annika Lindblom; Sara Margolin; Jenny Chang-Claude; Anja Rudolph; Paolo Radice; Laura Galastri; Janet E Olson; Emily Hallberg; Graham G Giles; Roger L Milne; Irene L Andrulis; Gord Glendon; Per Hall; Kamila Czene; Fiona Blows; Mitul Shah; Qin Wang; Joe Dennis; Kyriaki Michailidou; Lesley McGuffog; Manjeet K Bolla; Antonis C Antoniou; Douglas F Easton; Fergus J Couch; Sean Tavtigian; Maaike P Vreeswijk; Michael Parsons; Huong D Meeks; Alexandra Martins; David E Goldgar; Amanda B Spurdle
Journal:  Hum Mol Genet       Date:  2016-03-23       Impact factor: 6.150

10.  Splicing analysis for exonic and intronic mismatch repair gene variants associated with Lynch syndrome confirms high concordance between minigene assays and patient RNA analyses.

Authors:  Heleen M van der Klift; Anne M L Jansen; Niki van der Steenstraten; Elsa C Bik; Carli M J Tops; Peter Devilee; Juul T Wijnen
Journal:  Mol Genet Genomic Med       Date:  2015-04-23       Impact factor: 2.183

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