Specifications and validation of the ACMG/AMP criteria for clinical interpretation of sequence variants in collagen genes associated with joint hypermobility.
Journal
Human genetics
ISSN: 1432-1203
Titre abrégé: Hum Genet
Pays: Germany
ID NLM: 7613873
Informations de publication
Date de publication:
Jun 2023
Jun 2023
Historique:
received:
13
02
2023
accepted:
17
03
2023
medline:
15
5
2023
pubmed:
20
4
2023
entrez:
20
04
2023
Statut:
ppublish
Résumé
Deleterious variants in collagen genes are the most common cause of hereditary connective tissue disorders (HCTD). Adaptations of the American College of Medical Genetics and Genomics/Association for Molecular Pathology (ACMG/AMP) criteria are still lacking. A multidisciplinary team was set up for developing specifications of the ACMG/AMP criteria for COL1A1, COL1A2, COL2A1, COL3A1, COL5A1, COL5A2, COL11A1, COL11A2 and COL12A1, associated with various forms of HCTD featuring joint hypermobility, which is becoming one of the most common reasons of referral for molecular testing in this field. Such specifications were validated against 209 variants, and resulted effective for classifying as pathogenic and likely pathogenic null alleles without downgrading of the PVS1 level of strength and recurrent Glycine substitutions. Adaptations of selected criteria reduced uncertainties on private Glycine substitutions, intronic variants predicted to affect the splicing, and null alleles with a downgraded PVS1 level of strength. Segregation and multigene panel sequencing data mitigated uncertainties on non-Glycine substitutions by the attribution of one or more benignity criteria. These specifications may improve the clinical utility of molecular testing in HCTD by reducing the number of variants with neutral/conflicting interpretations. Close interactions between laboratory and clinicians are crucial to estimate the a priori utility of molecular test and to improve medical reports.
Identifiants
pubmed: 37079061
doi: 10.1007/s00439-023-02547-z
pii: 10.1007/s00439-023-02547-z
doi:
Substances chimiques
Collagen Type I, alpha2 Subunit
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
785-808Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Akawi NA, Al-Gazali L, Ali BR (2012) Clinical and molecular analysis of UAE fibrochondrogenesis patients expands the phenotype and reveals two COL11A1 homozygous null mutations. Clin Genet 82(2):147–156. https://doi.org/10.1111/j.1399-0004.2011.01734.x
doi: 10.1111/j.1399-0004.2011.01734.x
pubmed: 21668896
Bekdache GN, Begam MA, Chedid F, Al-Gazali L, Mirghani H (2013) Fibrochondrogenesis: prenatal diagnosis and outcome. J Obstet Gynaecol 33(7):663–668. https://doi.org/10.3109/01443615.2013.817977
doi: 10.3109/01443615.2013.817977
pubmed: 24127948
Biesecker LG, Harrison SM, ClinGen Sequence Variant Interpretation Working (2018) The ACMG/AMP reputable source criteria for the interpretation of sequence variants. Genet Med 20(12):1687–1688. https://doi.org/10.1038/gim.2018.42
doi: 10.1038/gim.2018.42
pubmed: 29543229
pmcid: 6709533
Brnich SE, Abou Tayoun AN, Couch FJ, Cutting GR, Greenblatt MS, Heinen CD, Kanavy DM, Luo X, McNulty SM, Starita LM, Tavtigian SV, Wright MW, Harrison SM, Biesecker LG, Clinical Berg JS, Genome Resource Sequence Variant Interpretation Working (2019) Recommendations for application of the functional evidence PS3/BS3 criterion using the ACMG/AMP sequence variant interpretation framework. Genome Med 12(1):3. https://doi.org/10.1186/s13073-019-0690-2
doi: 10.1186/s13073-019-0690-2
pubmed: 31892348
pmcid: 6938631
Chen JM, Masson E, Zou WB, Liao Z, Génin E, Cooper DN, Férec C (2023) Validation of the ACMG/AMP guidelines-based seven-category variant classification system. medRxiv. https://doi.org/10.1101/2023.01.23.23284909
doi: 10.1101/2023.01.23.23284909
pubmed: 37163006
pmcid: 10168412
Colman M, Castori M, Micale L, Ritelli Colombi M, Ghali N, Van Dijk F, Marsili L, Weeks A, Vandersteen A, Rideout A, Legrand A, Frank M, Mirault T, Ferraris A, Di Giosaffatte N, Grammatico P, Grunert J, Frank C, Symoens S, Syx D, Malfait F (2022) Atypical variants in COL1A1 and COL3A1 associated with classical and vascular Ehlers-Danlos syndrome overlap phenotypes: expanding the clinical phenotype based on additional case reports. Clin Exp Rheumatol 134(5):46–62. https://doi.org/10.55563/clinexprheumatol/kzkq6y
doi: 10.55563/clinexprheumatol/kzkq6y
Ewans LJ, Colley A, Gaston-Massuet C, Gualtieri A, Cowley MJ, McCabe MJ, Anand D, Lachke SA, Scietti L, Forneris F, Zhu Y, Ying K, Walsh C, Kirk EP, Miller D, Giunta C, Sillence D, Dinger M, Buckley M, Roscioli T (2019) Pathogenic variants in PLOD3 result in a Stickler syndrome-like connective tissue disorder with vascular complications. J Med Genet 56(9):629–638. https://doi.org/10.1136/jmedgenet-2019-106019
doi: 10.1136/jmedgenet-2019-106019
pubmed: 31129566
Ghosh R, Harrison SM, Rehm HL, Plon SE, Biesecker LG, ClinGen, Sequence Variant Interpretation Working (2018) Updated recommendation for the benign stand-alone ACMG/AMP criterion. Hum Mutat 39(11):1525–1530. https://doi.org/10.1002/humu.23642
doi: 10.1002/humu.23642
pubmed: 30311383
pmcid: 6188666
Heyne HO, Karjalainen J, Karczewski KJ, Lemmelä SM, Zhou W, FinnGen, Havulinna AS, Kurki M, Rehm HL, Palotie A, Daly MJ (2023) Mono- and biallelic variant effects on disease at biobank scale. Nature 613(7944):519–525. https://doi.org/10.1038/s41586-022-05420-7
doi: 10.1038/s41586-022-05420-7
pubmed: 36653560
pmcid: 9849130
Kelly MA, Caleshu C, Morales A, Buchan J, Wolf Z, Harrison SM, Cook S, Dillon MW, Garcia J, Haverfield E, Jongbloed JDH, Macaya D, Manrai A, Orland K, Richard G, Spoonamore K, Thomas M, Thomson K, Vincent LM, Walsh R, Watkins H, Whiffin N, Ingles J, van Tintelen JP, Semsarian C, Ware JS, Hershberger R, Funke B (2018) Adaptation and validation of the ACMG/AMP variant classification framework for MYH7-associated inherited cardiomyopathies: recommendations by ClinGen’s Inherited Cardiomyopathy Expert Panel. Genet Med 20(3):351–359. https://doi.org/10.1038/gim.2017.218
doi: 10.1038/gim.2017.218
pubmed: 29300372
pmcid: 5876064
Malfait F, Wenstrup R, De Paepe A (2007) Classic Ehlers-Danlos Syndrome. In: Adam MP, Mirzaa GM, Pagon RA, Wallace SE, Bean LJH, Gripp KW, Amemiya A (eds) GeneReviews® [Internet]. Seattle (WA): University of Washington, Seattle. PMID: 20301422
Malfait F, Symoens S, Goemans N, Gyftodimou Y, Holmberg E, Lopez-Gonzalez V, Mortier G, Nampoothiri S, Petersen MB, De Paepe A (2013) Helical mutations in type I collagen that affect the processing of the amino-propeptide result in an Osteogenesis Imperfecta/Ehlers-Danlos Syndrome overlap syndrome. Orphanet J Rare Dis 8:78. https://doi.org/10.1186/1750-1172-8-78
doi: 10.1186/1750-1172-8-78
pubmed: 23692737
pmcid: 3662563
Masson E, Zou WB, Génin E, Cooper DN, Le Gac G, Fichou Y, Pu N, Rebours V, Férec C, Liao Z, Chen JM (2022) Expanding ACMG variant classification guidelines into a general framework. Hum Genomics 16(1):31. https://doi.org/10.1186/s40246-022-00407-x
doi: 10.1186/s40246-022-00407-x
pubmed: 35974416
pmcid: 9380380
Micale L, Morlino S, Schirizzi A, Agolini E, Nardella G, Fusco C, Castellana S, Guarnieri V, Villa R, Bedeschi MF, Grammatico P, Novelli A, Castori M (2020) Exon-trapping assay improves clinical interpretation of COL11A1 and COL11A2 intronic variants in stickler syndrome type 2 and otospondylomegaepiphyseal dysplasia. Genes (Basel). https://doi.org/10.3390/genes11121513
doi: 10.3390/genes11121513
pubmed: 33348901
Morlino S, Micale L, Ritelli M, Rohrbach M, Zoppi N, Vandersteen A, Mackay S, Agolini E, Cocciadiferro D, Sasaki E, Madeo A, Ferraris A, Reardon W, Di Rocco M, Novelli A, Grammatico P, Malfait F, Mazza T, Hakim A, Giunta C, Colombi M, Castori M (2020) COL1-related overlap disorder: A novel connective tissue disorder incorporating the osteogenesis imperfecta/Ehlers-Danlos syndrome overlap. Clin Genet 97(3):396–406
doi: 10.1111/cge.13683
pubmed: 31794058
Oza AM, DiStefano MT, Hemphill SE, Cushman BJ, Grant AR, Siegert RK, Shen J, Chapin A, Boczek NJ, Schimmenti LA, Murry JB, Hasadsri L, Nara K, Kenna M, Booth KT, Azaiez H, Griffith A, Avraham KB, Kremer H, Rehm HL, Amr SS, Abou Tayoun AN, G. ClinGen Hearing Loss Clinical Domain Working (2018) Expert specification of the ACMG/AMP variant interpretation guidelines for genetic hearing loss. Hum Mutat 39(11):1593–1613. https://doi.org/10.1002/humu.23630
doi: 10.1002/humu.23630
pubmed: 30311386
pmcid: 6188673
Richards S, Aziz N, Bale S, Bick D, Das S, Gastier-Foster J, Grody WW, Hegde M, Lyon E, Spector E, Voelkerding K, Rehm HL, ALQA Committee (2015) Standards and guidelines for the interpretation of sequence variants: a joint consensus recommendation of the American College of Medical Genetics and Genomics and the Association for Molecular Pathology. Genet Med 17(5):405–424. https://doi.org/10.1038/gim.2015.30
doi: 10.1038/gim.2015.30
pubmed: 25741868
pmcid: 4544753
Savige J, Storey H, Watson E, Hertz JM, Deltas C, Renieri A, Mari F, Hilbert P, Plevova P, Byers P, Cerkauskaite A, Gregory M, Cerkauskiene R, Ljubanovic DG, Becherucci F, Errichiello C, Massella L, Aiello V, Lennon R, Hopkinson L, Koziell A, Lungu A, Rothe HM, Hoefele J, Zacchia M, Martic TN, Gupta A, van Eerde A, Gear S, Landini S, Palazzo V, Al-Rabadi L, Claes K, Corveleyn A, Van Hoof E, van Geel M, Williams M, Ashton E, Belge H, Ars E, Bierzynska A, Gangemi C, Lipska-Zietkiewicz BS (2021) Consensus statement on standards and guidelines for the molecular diagnostics of Alport syndrome: refining the ACMG criteria. Eur J Hum Genet 29(8):1186–1197. https://doi.org/10.1038/s41431-021-00858-1
doi: 10.1038/s41431-021-00858-1
pubmed: 33854215
pmcid: 8384871
Tavtigian SV, Greenblatt MS, Harrison SM, Nussbaum RL, Prabhu SA, Boucher KM, Biesecker LG, G. ClinGen Sequence Variant Interpretation Working (2018) Modeling the ACMG/AMP variant classification guidelines as a Bayesian classification framework. Genet Med 20(9):1054–1060. https://doi.org/10.1038/gim.2017.210
doi: 10.1038/gim.2017.210
pubmed: 29300386
pmcid: 6336098
Tavtigian SV, Harrison SM, Boucher KM, Biesecker LG (2020) Fitting a naturally scaled point system to the ACMG/AMP variant classification guidelines. Hum Mutat 41(10):1734–1737. https://doi.org/10.1002/humu.24088
doi: 10.1002/humu.24088
pubmed: 32720330
pmcid: 8011844