TY - JOUR
T1 - The different clinical facets of SYN1-related neurodevelopmental disorders
AU - Parenti, Ilaria
AU - Leitão, Elsa
AU - Kuechler, Alma
AU - Villard, Laurent
AU - Goizet, Cyril
AU - Courdier, Cécile
AU - Bayat, Allan
AU - Rossi, Alessandra
AU - Julia, Sophie
AU - Bruel, Ange-Line
AU - Tran Mau-Them, Frédéric
AU - Nambot, Sophie
AU - Lehalle, Daphné
AU - Willems, Marjolaine
AU - Lespinasse, James
AU - Ghoumid, Jamal
AU - Caumes, Roseline
AU - Smol, Thomas
AU - El Chehadeh, Salima
AU - Schaefer, Elise
AU - Abi-Warde, Marie-Thérèse
AU - Keren, Boris
AU - Afenjar, Alexandra
AU - Tabet, Anne-Claude
AU - Levy, Jonathan
AU - Maruani, Anna
AU - Aledo-Serrano, Ángel
AU - Garming, Waltraud
AU - Milleret-Pignot, Clara
AU - Chassevent, Anna
AU - Koopmans, Marije
AU - Verbeek, Nienke E
AU - Person, Richard
AU - Belles, Rebecca
AU - Bellus, Gary
AU - Salbert, Bonnie A
AU - Kaiser, Frank J
AU - Mazzola, Laure
AU - Convers, Philippe
AU - Perrin, Laurine
AU - Piton, Amélie
AU - Wiegand, Gert
AU - Accogli, Andrea
AU - Brancati, Francesco
AU - Benfenati, Fabio
AU - Chatron, Nicolas
AU - Lewis-Smith, David
AU - Thomas, Rhys H
AU - Zara, Federico
AU - Striano, Pasquale
N1 - Funding Information:
This research was funded in whole, or in part, by the Wellcome Trust [203914/Z/16/Z] supporting DL-S. For the purpose of Open Access, the author has applied a CC BY public copyright license to any Author Accepted Manuscript version arising from this submission. CD is supported by Universitätsklinikum Essen and received grants from the Deutsche Forschungsgemeinschaft (DFG). AB is funded by a BRIDGE—Translational Excellence Programme grant funded by the Novo Nordisk Foundation, grant agreement number: NNF20SA0064340. FB received funding from the Italian Ministry of Health.
Funding Information:
We thank the patients and their families for participating to this study. We acknowledge support from the Open Access Publication Fund of the University of Duisburg-Essen. One patient included in this study was diagnosed thanks to Defidiag (NCT04154891), a study supported by The French Ministry of Health and the Agence Nationale de la Recherche (ANR-10-IAHU-01).
Publisher Copyright:
Copyright © 2022 Parenti, Leitão, Kuechler, Villard, Goizet, Courdier, Bayat, Rossi, Julia, Bruel, Tran Mau-Them, Nambot, Lehalle, Willems, Lespinasse, Ghoumid, Caumes, Smol, El Chehadeh, Schaefer, Abi-Warde, Keren, Afenjar, Tabet, Levy, Maruani, Aledo-Serrano, Garming, Milleret-Pignot, Chassevent, Koopmans, Verbeek, Person, Belles, Bellus, Salbert, Kaiser, Mazzola, Convers, Perrin, Piton, Wiegand, Accogli, Brancati, Benfenati, Chatron, Lewis-Smith, Thomas, Zara, Striano, Lesca and Depienne.
PY - 2022/12/8
Y1 - 2022/12/8
N2 - Synapsin-I (SYN1) is a presynaptic phosphoprotein crucial for synaptogenesis and synaptic plasticity. Pathogenic SYN1 variants are associated with variable X-linked neurodevelopmental disorders mainly affecting males. In this study, we expand on the clinical and molecular spectrum of the SYN1-related neurodevelopmental disorders by describing 31 novel individuals harboring 22 different SYN1 variants. We analyzed newly identified as well as previously reported individuals in order to define the frequency of key features associated with these disorders. Specifically, behavioral disturbances such as autism spectrum disorder or attention deficit hyperactivity disorder are observed in 91% of the individuals, epilepsy in 82%, intellectual disability in 77%, and developmental delay in 70%. Seizure types mainly include tonic-clonic or focal seizures with impaired awareness. The presence of reflex seizures is one of the most representative clinical manifestations related to SYN1. In more than half of the cases, seizures are triggered by contact with water, but other triggers are also frequently reported, including rubbing with a towel, fever, toothbrushing, fingernail clipping, falling asleep, and watching others showering or bathing. We additionally describe hyperpnea, emotion, lighting, using a stroboscope, digestive troubles, and defecation as possible triggers in individuals with SYN1 variants. The molecular spectrum of SYN1 variants is broad and encompasses truncating variants (frameshift, nonsense, splicing and start-loss variants) as well as non-truncating variants (missense substitutions and in-frame duplications). Genotype-phenotype correlation revealed that epileptic phenotypes are enriched in individuals with truncating variants. Furthermore, we could show for the first time that individuals with early seizures onset tend to present with severe-to-profound intellectual disability, hence highlighting the existence of an association between early seizure onset and more severe impairment of cognitive functions. Altogether, we present a detailed clinical description of the largest series of individuals with SYN1 variants reported so far and provide the first genotype-phenotype correlations for this gene. A timely molecular diagnosis and genetic counseling are cardinal for appropriate patient management and treatment.
AB - Synapsin-I (SYN1) is a presynaptic phosphoprotein crucial for synaptogenesis and synaptic plasticity. Pathogenic SYN1 variants are associated with variable X-linked neurodevelopmental disorders mainly affecting males. In this study, we expand on the clinical and molecular spectrum of the SYN1-related neurodevelopmental disorders by describing 31 novel individuals harboring 22 different SYN1 variants. We analyzed newly identified as well as previously reported individuals in order to define the frequency of key features associated with these disorders. Specifically, behavioral disturbances such as autism spectrum disorder or attention deficit hyperactivity disorder are observed in 91% of the individuals, epilepsy in 82%, intellectual disability in 77%, and developmental delay in 70%. Seizure types mainly include tonic-clonic or focal seizures with impaired awareness. The presence of reflex seizures is one of the most representative clinical manifestations related to SYN1. In more than half of the cases, seizures are triggered by contact with water, but other triggers are also frequently reported, including rubbing with a towel, fever, toothbrushing, fingernail clipping, falling asleep, and watching others showering or bathing. We additionally describe hyperpnea, emotion, lighting, using a stroboscope, digestive troubles, and defecation as possible triggers in individuals with SYN1 variants. The molecular spectrum of SYN1 variants is broad and encompasses truncating variants (frameshift, nonsense, splicing and start-loss variants) as well as non-truncating variants (missense substitutions and in-frame duplications). Genotype-phenotype correlation revealed that epileptic phenotypes are enriched in individuals with truncating variants. Furthermore, we could show for the first time that individuals with early seizures onset tend to present with severe-to-profound intellectual disability, hence highlighting the existence of an association between early seizure onset and more severe impairment of cognitive functions. Altogether, we present a detailed clinical description of the largest series of individuals with SYN1 variants reported so far and provide the first genotype-phenotype correlations for this gene. A timely molecular diagnosis and genetic counseling are cardinal for appropriate patient management and treatment.
KW - SYN1
KW - autism spectrum disorders
KW - genotype-phenotype correlation
KW - neurodevelopmental disorders
KW - reflex epilepsy
KW - synapsins
UR - http://www.scopus.com/inward/record.url?scp=85144967645&partnerID=8YFLogxK
U2 - 10.3389/fcell.2022.1019715
DO - 10.3389/fcell.2022.1019715
M3 - Article
C2 - 36568968
SN - 2296-634X
VL - 10
SP - 1
EP - 18
JO - Frontiers in Cell and Developmental Biology
JF - Frontiers in Cell and Developmental Biology
M1 - 1019715
ER -