SYT1-associated neurodevelopmental disorder: A case series

Brain

Volumn 141, Issue 9, 2018, Pages 2576-2591

  Baker, Kate ^a,b   Gordon, Sarah L ^c   Melland, Holly ^c   Bumbak, Fabian ^c   Scott, Daniel J ^c   Jiang, Tess J ^c   Owen, David ^a   Turner, Bradley J ^c   Boyd, Stewart G ^d   Rossi, Mari ^e   Al Raqad, Mohammed ^f   Elpeleg, Orly ^g   Peck, Dawn ^h   Mancini, Grazia M S ⁱ   Wilke, Martina ⁱ   Zollino, Marcella ^j   Marangi, Giuseppe ^j   Weigand, Heike ^k   Borggraefe, Ingo ^k   Haack, Tobias ^l,m   Stark, Zornitza ⁿ   Sadedin, Simon ^n,o   Genomics, Mendelian ^o   Tan, Tiong Yang ⁿ   Jiang, Yunyun ^p   Gibbs, Richard A ^p   Ellingwood, Sara ^q   Amaral, Michelle ^r   Kelley, Whitley ^r   Kurian, Manju A ^d   Cousin, Michael A ^s   Raymond, F Lucy ^a   more..

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MRC COGNITION AND BRAIN SCIENCES UNIT   (United Kingdom)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e AMBRY GENETICS   (United States)

^f Division of Pediatric Pulmonology   (Jordan)

^g HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^h UNIVERSITY OF MISSOURI   (United States)

ⁱ ERASMUS MEDICAL CENTER   (Netherlands)

^j CATHOLIC UNIVERSITY   (Italy)

^k LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^l TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^m UNIVERSITY OF TÜBINGEN   (Germany)

ⁿ MURDOCH CHILDREN'S RESEARCH INSTITUTE   (Australia)

^o BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^p BAYLOR COLLEGE OF MEDICINE   (United States)

^q Maine Medical Partners   (United States)

^r HUDSONALPHA INSTITUTE FOR BIOTECHNOLOGY   (United States)

^s UNIVERSITY OF EDINBURGH   (United Kingdom)

more..

Author keywords

intellectual disability; movement disorder; synaptic vesicle; synaptotagmin 1; SYT1

Indexed keywords

SYNAPTOTAGMIN I; CALCIUM; SYT1 PROTEIN, HUMAN; SYT1 PROTEIN, MOUSE; SYT1 PROTEIN, RAT;

ACTION POTENTIAL; ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATAXIA; CEREBRAL PALSY; CHILD; CHOREOATHETOSIS; CLINICAL ARTICLE; CLINICAL FEATURE; COGNITIVE DEVELOPMENT; CONTRACTURE; CONTROLLED STUDY; DEPOLARIZATION; FAMILY HISTORY; FOOT MALFORMATION; GENE MUTATION; HEART ATRIUM SEPTUM DEFECT; HUMAN; HUMAN CELL; HYPERKINESIA; INFANTILE HYPOTONIA; JOINT LAXITY; LARYNGOMALACIA; LORDOSIS; MEDICAL HISTORY; MENTAL DISEASE; MISSENSE MUTATION; MOLECULAR DYNAMICS; MOTOR DYSFUNCTION; NERVE CELL DIFFERENTIATION; NERVE ENDING; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROIMAGING; NEUROLOGIC DISEASE; NEUROTRANSMITTER RELEASE; NONHUMAN; PHYSICAL EXAMINATION; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RAT; SCHOOL CHILD; SCOLIOSIS; SYNAPSE VESICLE; SYNDACTYLY; TERATOMA; VALGUS DEFORMITY; YOUNG ADULT; ANIMAL; C57BL MOUSE; CASE REPORT; ELECTROPHYSIOLOGY; ENDOCYTOSIS; FEMALE; GENETICS; INTELLECTUAL IMPAIRMENT; MALE; METABOLISM; MOUSE; NERVE CELL; PHYSIOLOGY; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ADOLESCENT; ANIMALS; CALCIUM; CHILD; CHILD, PRESCHOOL; ELECTROPHYSIOLOGICAL PHENOMENA; ENDOCYTOSIS; FEMALE; HUMANS; INTELLECTUAL DISABILITY; MALE; MICE; MICE, INBRED C57BL; MOVEMENT DISORDERS; MUTATION, MISSENSE; NEURODEVELOPMENTAL DISORDERS; NEURONS; RATS; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; SYNAPTOTAGMIN I; YOUNG ADULT;

EID: 85058731148     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awy209     Document Type: Article

References (37)

1. Baker K, Gordon SL, Grozeva D, van Kogelenberg M, Roberts NY, Pike M, et al. Identification of a human synaptotagmin-1 mutation that perturbs synaptic vesicle cycling. J Clin Invest 2015; 125: 1670-8.
2. Bellus GA, Hefferon TW, Ortiz de Luna RI, Hecht JT, Horton WA, Machado M, et al. Achondroplasia is defined by recurrent G380R mutations of FGFR3. Am J Hum Genet 1995; 56: 368-73.
3. Blanchard MG, Willemsen MH, Walker JB, Dib-Hajj SD, Waxman SG, Jongmans MC, et al. De novo gain-of-function and loss-of-function mutations of SCN8A in patients with intellectual disabilities and epilepsy. J Med Genet 2015; 52: 330-7.
4. Cafiero C, Marangi G, Orteschi D, Ali M, Asaro A, Ponzi E, et al. Novel de novo heterozygous loss-of-function variants in MED13L and further delineation of the MED13L haploinsufficiency syndrome. Eur J Hum Genet 2015; 23: 1499-504.
5. Ebrahimi-Fakhari D, Saffari A, Westenberger A, Klein C. The evolving spectrum of PRRT2-associated paroxysmal diseases. Brain 2015; 138 (Pt 12): 3476-95.
6. Ferguson SM, Brasnjo G, Hayashi M, Wolfel M, Collesi C, Giovedi S, et al. A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 2007; 316: 570-4.
7. Gordon SL, Cousin MA. X-linked intellectual disability-associated mutations in synaptophysin disrupt synaptobrevin II retrieval. J Neurosci 2013; 33: 13695-700.
8. Gordon SL, Leube RE, Cousin MA. Synaptophysin is required for synaptobrevin retrieval during synaptic vesicle endocytosis. J Neurosci 2011; 31: 14032-6.
9. Hamdan FF, Myers CT, Cossette P, Lemay P, Spiegelman D, Laporte AD, et al. High rate of recurrent de novo mutations in developmental and epileptic encephalopathies. Am J Hum Genet 2017; 101: 664-85.
10. Herrmann DN, Horvath R, Sowden JE, Gonzalez M, Sanchez-Mejias A, Guan Z, et al. Synaptotagmin 2 mutations cause an autosomaldominant form of lambert-eaton myasthenic syndrome and nonprogressive motor neuropathy. Am J Hum Genet 2014; 95: 332-9.
11. Hui E, Johnson CP, Yao J, Dunning FM, Chapman ER. Synaptotagmin-mediated bending of the target membrane is a critical step in Ca(2 + )-regulated fusion. Cell 2009; 138: 709-21.
12. Jahn R, Fasshauer D. Molecular machines governing exocytosis of synaptic vesicles. Nature 2012; 490: 201-7.
13. Jay JJ, Brouwer C. Lollipops in the clinic: Information dense mutation plots for precision medicine. PLoS One 2016; 11: E0160519.
14. Kang HJ, Kawasawa YI, Cheng F, Zhu Y, Xu X, Li M, et al. Spatiotemporal transcriptome of the human brain. Nature 2011; 478: 483-9.
15. Kohler S, Vasilevsky NA, Engelstad M, Foster E, McMurry J, Ayme S, et al. The Human Phenotype Ontology in 2017. Nucleic Acids Res 2017; 45: D865-76.
16. Kwon SE, Chapman ER. Synaptophysin regulates the kinetics of synaptic vesicle endocytosis in central neurons. Neuron 2011; 70: 847-54.
17. Lek M, Karczewski KJ, Minikel EV, Samocha KE, Banks E, Fennell T, et al. Analysis of protein-coding genetic variation in 60 706 humans. Nature 2016; 536: 285-91.
18. Lipstein N, Verhoeven-Duif NM, Michelassi FE, Calloway N, van Hasselt PM, Pienkowska K, et al. Synaptic UNC13A protein variant causes increased neurotransmission and dyskinetic movement disorder. J Clin Invest 2017; 127: 1005-18.
19. Lyles V, Zhao Y, Martin KC. Synapse formation and mRNA localization in cultured Aplysia neurons. Neuron 2006; 49: 349-56.
20. Mackler JM, Drummond JA, Loewen CA, Robinson IM, Reist NE. The C(2)B Ca(2 + )-binding motif of synaptotagmin is required for synaptic transmission in vivo. Nature 2002; 418: 340-4.
21. Martens S, Kozlov MM, McMahon HT. How synaptotagmin promotes membrane fusion. Science 2007; 316: 1205-8.
22. McNicholas S, Potterton E, Wilson KS, Noble ME. Presenting your structures: The CCP4mg molecular-graphics software. Acta Crystallogr D Biol Crystallogr 2011; 67 (Pt 4): 386-94.
23. Mendez JA, Bourque MJ, Fasano C, Kortleven C, Trudeau LE. Somatodendritic dopamine release requires synaptotagmin 4 and 7 and the participation of voltage-gated calcium channels. J Biol Chem 2011; 286: 23928-37.
24. Nishiki T, Augustine GJ. Dual roles of the C2B domain of synaptotagmin I in synchronizing Ca2 + -dependent neurotransmitter release. J Neurosci 2004; 24: 8542-50.
25. Paddock BE, Wang Z, Biela LM, Chen K, Getzy MD, Striegel A, et al. Membrane penetration by synaptotagmin is required for coupling calcium binding to vesicle fusion in vivo. J Neurosci 2011; 31: 2248-57.
26. Poskanzer KE, Marek KW, Sweeney ST, Davis GW. Synaptotagmin I is necessary for compensatory synaptic vesicle endocytosis in vivo. Nature 2003; 426: 559-63.
27. Sudhof TC. Neurotransmitter release: The last millisecond in the life of a synaptic vesicle. Neuron 2013; 80: 675-90.
28. Tarpey PS, Smith R, Pleasance E, Whibley A, Edkins S, Hardy C, et al. A systematic, large-scale resequencing screen of X-chromosome coding exons in mental retardation. Nat Genet 2009; 41: 535-43.
29. Valtorta F, Benfenati F, Zara F, Meldolesi J. PRRT2: From paroxysmal disorders to regulation of synaptic function. Trends Neurosci 2016; 39: 668-79.
30. von Spiczak S, Helbig KL, Shinde DN, Huether R, Pendziwiat M, Lourenco C, et al. DNM1 encephalopathy: A new disease of vesicle fission. Neurology 2017; 89: 385-94.
31. Waites CL, Garner CC. Presynaptic function in health and disease. Trends Neurosci 2011; 34: 326-37.
32. Warner TA, Shen W, Huang X, Liu Z, Macdonald RL, Kang JQ. Differential molecular and behavioural alterations in mouse models of GABRG2 haploinsufficiency versus dominant negative mutations associated with human epilepsy. Hum Mol Genet 2016; 25: 3192-207.
33. Whittaker RG, Herrmann DN, Bansagi B, Hasan BA, Lofra RM, Logigian EL, et al. Electrophysiologic features of SYT2 mutations causing a treatable neuromuscular syndrome. Neurology 2015; 85: 1964-71.
34. Wu D, Bacaj T, Morishita W, Goswami D, Arendt KL, Xu W, et al. Postsynaptic synaptotagmins mediate AMPA receptor exocytosis during LTP. Nature 2017; 544: 316-21.
35. Yao J, Kwon SE, Gaffaney JD, Dunning FM, Chapman ER. Uncoupling the roles of synaptotagmin I during endo- and exocytosis of synaptic vesicles. Nat Neurosci 2011; 15: 243-9.
36. Zhou Q, Lai Y, Bacaj T, Zhao M, Lyubimov AY, Uervirojnangkoorn M, et al. Architecture of the synaptotagmin-SNARE machinery for neuronal exocytosis. Nature 2015; 525: 62-7.
37. Zhou Q, Zhou P, Wang AL, Wu D, Zhao M, Sudhof TC, et al. The primed SNARE-complexin-synaptotagmin complex for neuronal exocytosis. Nature 2017; 548: 420-5.