TY - JOUR
T1 - Biallelic loss of function variants in SYT2 cause a treatable congenital onset presynaptic myasthenic syndrome
AU - Donkervoort, Sandra
AU - Mohassel, Payam
AU - Laugwitz, Lucia
AU - Zaki, Maha S.
AU - Kamsteeg, Erik Jan
AU - Maroofian, Reza
AU - Chao, Katherine R.
AU - Verschuuren-Bemelmans, Corien C.
AU - Horber, Veronka
AU - Fock, Annemarie J.M.
AU - McCarty, Riley M.
AU - Jain, Minal S.
AU - Biancavilla, Victoria
AU - McMacken, Grace
AU - Nalls, Matthew
AU - Voermans, Nicol C.
AU - Elbendary, Hasnaa M.
AU - Snyder, Molly
AU - Cai, Chunyu
AU - Lehky, Tanya J.
AU - Stanley, Valentina
AU - Iannaccone, Susan T.
AU - Foley, A. Reghan
AU - Lochmüller, Hanns
AU - Gleeson, Joseph
AU - Houlden, Henry
AU - Haack, Tobias B.
AU - Horvath, Rita
AU - Bönnemann, Carsten G.
N1 - Funding Information:
We thank the patients and their families for participating in our research study and Christopher Mendoza, Christine Jones, and Gilberto (“Mike”) Averion for their help in clinic. We also thank the Genome Aggregation Database (gnomAD) and the groups that provided exome and genome variant data to this resource. A full list of contributing groups can be found at https://gnomad.broadinstitute.org/about . The work in C.G. Bönnemann's laboratory is supported by intramural funds from the NIH National Institute of Neurological Disorders and Stroke. R. H. is a Wellcome Trust Investigator (109915/Z/15/Z), who receives support from the Medical Research Council (UK) (MR/N025431/1), the European Research Council (309548), the Wellcome Trust Pathfinder Scheme (201064/Z/16/Z) and the Newton Fund (UK/Turkey, MR/N027302/1). H. L. is the recipient of a Canadian Institutes of Health Research Foundation Grant (CIHR FDN‐167281). Sequencing and analysis were provided by the Broad Institute of MIT and Harvard Center for Mendelian Genomics (Broad CMG) and was funded by the National Human Genome Research Institute, the National Eye Institute, and the National Heart, Lung and Blood Institute grant UM1 HG008900 to Daniel MacArthur and Heidi Rehm.
Funding Information:
Canadian Institutes of Health Research Foundation Grant, Grant/Award Number: CIHR FDN‐167281; European Research Council, Grant/Award Number: 309548; Medical Research Council, Grant/Award Number: MR/N025431/1; National Human Genome Research Institute, Grant/Award Number: R01 HG009141; National Human Genome Research Institute, the National Eye Institute, and the National Heart, Lung and Blood Institute, Grant/Award Number: UM1 HG008900; Newton Fund, UK/Turkey, Grant/Award Number: MR/N027302/1; Wellcome Trust Investigator, Grant/Award Number: 109915/Z/15/Z; Wellcome Trust Pathfinder Scheme, Grant/Award Number: 201064/Z/16/Z Funding information
Funding Information:
We thank the patients and their families for participating in our research study and Christopher Mendoza, Christine Jones, and Gilberto (?Mike?) Averion for their help in clinic. We also thank the Genome Aggregation Database (gnomAD) and the groups that provided exome and genome variant data to this resource. A full list of contributing groups can be found at https://gnomad.broadinstitute.org/about. The work in C.G. B?nnemann's laboratory is supported by intramural funds from the NIH National Institute of Neurological Disorders and Stroke. R. H. is a Wellcome Trust Investigator (109915/Z/15/Z), who receives support from the Medical Research Council (UK) (MR/N025431/1), the European Research Council (309548), the Wellcome Trust Pathfinder Scheme (201064/Z/16/Z) and the Newton Fund (UK/Turkey, MR/N027302/1). H. L. is the recipient of a Canadian Institutes of Health Research Foundation Grant (CIHR FDN-167281). Sequencing and analysis were provided by the Broad Institute of MIT and Harvard Center for Mendelian Genomics (Broad CMG) and was funded by the National Human Genome Research Institute, the National Eye Institute, and the National Heart, Lung and Blood Institute grant UM1 HG008900 to Daniel MacArthur and Heidi Rehm.
Publisher Copyright:
© 2020 Wiley Periodicals LLC
PY - 2020/10/1
Y1 - 2020/10/1
N2 - Synaptotagmins are integral synaptic vesicle membrane proteins that function as calcium sensors and regulate neurotransmitter release at the presynaptic nerve terminal. Synaptotagmin-2 (SYT2), is the major isoform expressed at the neuromuscular junction. Recently, dominant missense variants in SYT2 have been reported as a rare cause of distal motor neuropathy and myasthenic syndrome, manifesting with stable or slowly progressive distal weakness of variable severity along with presynaptic NMJ impairment. These variants are thought to have a dominant-negative effect on synaptic vesicle exocytosis, although the precise pathomechanism remains to be elucidated. Here we report seven patients of five families, with biallelic loss of function variants in SYT2, clinically manifesting with a remarkably consistent phenotype of severe congenital onset hypotonia and weakness, with variable degrees of respiratory involvement. Electrodiagnostic findings were consistent with a presynaptic congenital myasthenic syndrome (CMS) in some. Treatment with an acetylcholinesterase inhibitor pursued in three patients showed clinical improvement with increased strength and function. This series further establishes SYT2 as a CMS-disease gene and expands its clinical and genetic spectrum to include recessive loss-of-function variants, manifesting as a severe congenital onset presynaptic CMS with potential treatment implications.
AB - Synaptotagmins are integral synaptic vesicle membrane proteins that function as calcium sensors and regulate neurotransmitter release at the presynaptic nerve terminal. Synaptotagmin-2 (SYT2), is the major isoform expressed at the neuromuscular junction. Recently, dominant missense variants in SYT2 have been reported as a rare cause of distal motor neuropathy and myasthenic syndrome, manifesting with stable or slowly progressive distal weakness of variable severity along with presynaptic NMJ impairment. These variants are thought to have a dominant-negative effect on synaptic vesicle exocytosis, although the precise pathomechanism remains to be elucidated. Here we report seven patients of five families, with biallelic loss of function variants in SYT2, clinically manifesting with a remarkably consistent phenotype of severe congenital onset hypotonia and weakness, with variable degrees of respiratory involvement. Electrodiagnostic findings were consistent with a presynaptic congenital myasthenic syndrome (CMS) in some. Treatment with an acetylcholinesterase inhibitor pursued in three patients showed clinical improvement with increased strength and function. This series further establishes SYT2 as a CMS-disease gene and expands its clinical and genetic spectrum to include recessive loss-of-function variants, manifesting as a severe congenital onset presynaptic CMS with potential treatment implications.
KW - SYT2
KW - congenital myasthenic syndrome
KW - neuromuscular junction
KW - presynaptic CMS
KW - synaptotagmins
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U2 - 10.1002/ajmg.a.61765
DO - 10.1002/ajmg.a.61765
M3 - Article
C2 - 32776697
AN - SCOPUS:85089152001
SN - 1552-4825
VL - 182
SP - 2272
EP - 2283
JO - American Journal of Medical Genetics, Part A
JF - American Journal of Medical Genetics, Part A
IS - 10
ER -