TY - JOUR
T1 - Mutation-specific pathophysiological mechanisms define different neurodevelopmental disorders associated with SATB1 dysfunction
AU - The DDD study
AU - den Hoed, Joery
AU - de Boer, Elke
AU - Voisin, Norine
AU - Dingemans, Alexander J.M.
AU - Guex, Nicolas
AU - Wiel, Laurens
AU - Nellaker, Christoffer
AU - Amudhavalli, Shivarajan M.
AU - Banka, Siddharth
AU - Bena, Frederique S.
AU - Ben-Zeev, Bruria
AU - Bonagura, Vincent R.
AU - Bruel, Ange Line
AU - Brunet, Theresa
AU - Brunner, Han G.
AU - Chew, Hui B.
AU - Chrast, Jacqueline
AU - Cimbalistienė, Loreta
AU - Coon, Hilary
AU - Délot, Emmanuèlle C.
AU - Démurger, Florence
AU - Denommé-Pichon, Anne Sophie
AU - Depienne, Christel
AU - Donnai, Dian
AU - Dyment, David A.
AU - Elpeleg, Orly
AU - Faivre, Laurence
AU - Gilissen, Christian
AU - Granger, Leslie
AU - Haber, Benjamin
AU - Hachiya, Yasuo
AU - Abedi, Yasmin Hamzavi
AU - Hanebeck, Jennifer
AU - Hehir-Kwa, Jayne Y.
AU - Horist, Brooke
AU - Itai, Toshiyuki
AU - Jackson, Adam
AU - Jewell, Rosalyn
AU - Jones, Kelly L.
AU - Joss, Shelagh
AU - Kashii, Hirofumi
AU - Kato, Mitsuhiro
AU - Kattentidt-Mouravieva, Anja A.
AU - Kok, Fernando
AU - Kotzaeridou, Urania
AU - Krishnamurthy, Vidya
AU - Kučinskas, Vaidutis
AU - Kuechler, Alma
AU - Lavillaureix, Alinoë
AU - Willing, Marcia
N1 - Funding Information:
We are extremely grateful to all families participating in this study. In addition, we wish to thank the members of the Genome Technology Center and Cell culture facility, Department of Human Genetics, Radboud university medical center, Nijmegen, for data processing and cell culture of proband-derived cell lines. This work was financially supported by Aspasia grants of the Dutch Research Council ( 015.014.036 to T.K. and 015.014.066 to L.E.L.M.V.), Netherlands Organization for Health Research and Development ( 91718310 to T.K.), the Max Planck Society (J.d.H., S.E.F.), Oxford Brookes University , the Leverhulme Trust , and the British Academy (D.F.N.), and grants from the Swiss National Science Foundation ( 31003A_182632 to A.R.), Lithuanian-Swiss cooperation program to reduce economic and social disparities within the enlarged European Union (A.R., V. Kučinskas) and the Jérôme Lejeune Foundation (A.R.). We wish to acknowledge ALSPAC, the UK10K consortium, the 100,000 Genomes Project, “TRANSLATE NAMSE,” and Genomic Answers for Kids program (see supplemental acknowledgments ). In addition, the collaborations in this study were facilitated by ERN ITHACA, one of the 24 European Reference Networks (ERNs) approved by the ERN Board of Member States, co-funded by European Commission. The aims of this study contribute to the Solve-RD project (E.d.B., H.G.B., S.B., A.-S.D.-P., L.F., C.G., A.J., T.K., A.V., L.E.L.M.V.), which has received funding from the European Union’s Horizon 2020 research and innovation program under grant agreement No 779257 .
Funding Information:
We are extremely grateful to all families participating in this study. In addition, we wish to thank the members of the Genome Technology Center and Cell culture facility, Department of Human Genetics, Radboud university medical center, Nijmegen, for data processing and cell culture of proband-derived cell lines. This work was financially supported by Aspasia grants of the Dutch Research Council (015.014.036 to T.K. and 015.014.066 to L.E.L.M.V.), Netherlands Organization for Health Research and Development (91718310 to T.K.), the Max Planck Society (J.d.H. S.E.F.), Oxford Brookes University, the Leverhulme Trust, and the British Academy (D.F.N.), and grants from the Swiss National Science Foundation (31003A_182632 to A.R.), Lithuanian-Swiss cooperation program to reduce economic and social disparities within the enlarged European Union (A.R. V. Ku?inskas) and the J?r?me Lejeune Foundation (A.R.). We wish to acknowledge ALSPAC, the UK10K consortium, the 100,000 Genomes Project, ?TRANSLATE NAMSE,? and Genomic Answers for Kids program (see supplemental acknowledgments). In addition, the collaborations in this study were facilitated by ERN ITHACA, one of the 24 European Reference Networks (ERNs) approved by the ERN Board of Member States, co-funded by European Commission. The aims of this study contribute to the Solve-RD project (E.d.B. H.G.B. S.B. A.-S.D.-P. L.F. C.G. A.J. T.K. A.V. L.E.L.M.V.), which has received funding from the European Union's Horizon 2020 research and innovation program under grant agreement No 779257.
Publisher Copyright:
© 2021 American Society of Human Genetics
PY - 2021/2/4
Y1 - 2021/2/4
N2 - Whereas large-scale statistical analyses can robustly identify disease-gene relationships, they do not accurately capture genotype-phenotype correlations or disease mechanisms. We use multiple lines of independent evidence to show that different variant types in a single gene, SATB1, cause clinically overlapping but distinct neurodevelopmental disorders. Clinical evaluation of 42 individuals carrying SATB1 variants identified overt genotype-phenotype relationships, associated with different pathophysiological mechanisms, established by functional assays. Missense variants in the CUT1 and CUT2 DNA-binding domains result in stronger chromatin binding, increased transcriptional repression, and a severe phenotype. In contrast, variants predicted to result in haploinsufficiency are associated with a milder clinical presentation. A similarly mild phenotype is observed for individuals with premature protein truncating variants that escape nonsense-mediated decay, which are transcriptionally active but mislocalized in the cell. Our results suggest that in-depth mutation-specific genotype-phenotype studies are essential to capture full disease complexity and to explain phenotypic variability.
AB - Whereas large-scale statistical analyses can robustly identify disease-gene relationships, they do not accurately capture genotype-phenotype correlations or disease mechanisms. We use multiple lines of independent evidence to show that different variant types in a single gene, SATB1, cause clinically overlapping but distinct neurodevelopmental disorders. Clinical evaluation of 42 individuals carrying SATB1 variants identified overt genotype-phenotype relationships, associated with different pathophysiological mechanisms, established by functional assays. Missense variants in the CUT1 and CUT2 DNA-binding domains result in stronger chromatin binding, increased transcriptional repression, and a severe phenotype. In contrast, variants predicted to result in haploinsufficiency are associated with a milder clinical presentation. A similarly mild phenotype is observed for individuals with premature protein truncating variants that escape nonsense-mediated decay, which are transcriptionally active but mislocalized in the cell. Our results suggest that in-depth mutation-specific genotype-phenotype studies are essential to capture full disease complexity and to explain phenotypic variability.
KW - HPO-based analysis
KW - SATB1
KW - cell-based functional assays
KW - de novo variants
KW - intellectual disability
KW - neurodevelopmental disorders
KW - seizures
KW - teeth abnormalities
UR - http://www.scopus.com/inward/record.url?scp=85100239938&partnerID=8YFLogxK
U2 - 10.1016/j.ajhg.2021.01.007
DO - 10.1016/j.ajhg.2021.01.007
M3 - Article
C2 - 33513338
AN - SCOPUS:85100239938
VL - 108
SP - 346
EP - 356
JO - American Journal of Human Genetics
JF - American Journal of Human Genetics
SN - 0002-9297
IS - 2
ER -