Synaptotagmin 2 Mutations Cause Autosomal-Dominant Form of Lambert-Eaton Myasthenic Syndrome and Nonprogressive Motor Neuropathy
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1 The American Journal of Human Genetics, Volume 95 Supplemental Data Synaptotagmin 2 Mutations Cause AutosomalDominant Form of LambertEaton Myasthenic Syndrome and Nonprogressive Motor Neuropathy David N. Herrmann, Rita Horvath, Janet E. Sowden, Michael Gonzales, Avencia SanchezMejias, Zhuo Guan, Roger G. Whittaker, Jorge L. Almodovar, Maria Lane, Boglarka Bansagi, Angela Pyle, Veronika Boczonadi, Hanns Lochmüller, Helen Griffin, Patrick F. Chinnery, Thomas E. Lloyd, J. Troy Littleton, and Stephan Zuchner
2 Figure S1 A Glu424 C2B loop 3 op 3 Asp Ca Asp361 Asp Ca B Asp307 C2B l C2B loop 1 M V S E S H H E A L A A P P V T T M R N I F K R N Q E P I V A P A T T T MP P N A K S E T D A K P E A E P A P A S E P A A D L E S V D Q K L E E T H H S K F R E V D R Q E Q E V L A E K A A E A V A T V L P S N A T E P A S P G E G K E D A F S K L K E K F MN E L H K I P L P P WA L I A I A A T MP I G P V D N S T E S G G A G E S Q E D M F A K L K E K L F N E I N K I P L P P WA L I A I A A S Q R I A Q V E S T T R S A T T E A Q E S T T T A V P V I K K I E H V G E V V T E V I A E R T G L P T WG V V A I I I V A V L L V L T C C F C I C K K C L F K K K N K K K G K E K G G K N A I N MK D V K D L G K T MK D Q A L K D D D A E V V A G L L L L T C C F C I C K K C C C K K K K N K K E K G K G MK N A MN MK DMK G G Q D D D D A E I L V F L V V F G I I F F C V R R F L K K R R T K D G K G K K G V DMK S V Q L L G S A Y K E K V Q P DME E L * * T G L T D G E E K E E P K E E E K L G K L Q Y S L D Y D F Q N N Q L L V G I I Q A A E L P A L DM G G T S D P Y V K V T G L T E G E G E G E E E K E P E N L G K L Q F S L D Y D F Q A N Q L T V G V L Q A A E L P A L DM G G T S D P Y V K V T E N A E E G D E E D K Q S E Q K L G R L N F K L E Y D F N S N S L A V T V I Q A E E L P A L DM G G T S D P Y V K V * * * F L L P D K K K K F E T K V H R K T L N P V F N E Q F T F K V P Y S E L G G K T L V MA V Y D F D R F S K H D I I G E F L L P D K K K K Y E T K V H R K T L N P A F N E T F T F K V P Y Q E L G G K T L V MA I Y D F D R F S K H D I I G E Y L L P D K K K K F E T K V H R K T L S P V F N E T F T F K S L P Y A D A MN K T L V F A I F D F D R F S K H D Q I G E F K V P MN T V D F G H V T E E WR D L Q S A E K E E Q E K L G D I C F S L R Y V P T A G K L T V V I L E A K N L K K V K V P MN T V D L G Q P I E E WR D L Q G G E K E E P E K L G D I C T S L R Y V P T A G K L T V C I L E A K N L K K V K V P L C T I D L A Q T I E E WR D L V S V E G E G G Q E K L G D I C F S L R Y V P T A G K L T V V I L E A K N L K K * * MD V G G L S D P Y V K I H L MQ N G K R L K K K K T T I K K N T L N P Y Y N E S F S F E V P F E Q I Q K V Q V V V T V MD V G G L S D P Y V K I H L MQ N G K R L K K K K T T V K K K T L N P Y F N E S F S F E I P F E Q I Q K V Q V V V T V MD V G G L S D P Y V K I A I MQ N G K R L K K K K T S I K K C T L N P Y Y N E S F S F E V P F E Q I Q K I C L V V T V * * * L D Y D K I G K N D A I G K V F V G Y N S T G A E L R HWS DML A N P R R P I A QWH T L Q V E E E V D A ML A V K K L D Y D K L G K N E A I G K I F V G S N A T G T E L R HWS DML A N P R R P I A QWH S L K P E E E V D A L L G K N K V D Y D R I G T S E P I G R C I L G C M G T G T E L R HWS DML A S P R R P I A QWH T L K D P E E T D E I L K N MK
3 Figure S1. Conservation of human SYT2 and Drosophila SYT1. (A) Schematic diagram of the key residues (green) that protrude from the top of the C2B domain that coordinate calcium binding in SYT2 (diagram based on Fernandez et. al. 1 ). The Asp307 residue is highlighted in orange. (B) Alignment of amino acid sequences of human SYT1, human SYT2 and Drosophila SYT1, highlighting the conservation between the synaptic vesicle SYT isoforms. The transmembrane domain and the C2A and C2B calcium binding domains are highlighted in black, purple, and blue boxes, respectively. The five key aspartate (D) residues that mediate calcium binding to each C2 domain are indicated with green asterisks. The fifth aspartate reside in C2B in human SYT1 is replaced by a glutamate residue in human SYT2 and Drosophila SYT1. The Asp307 residue (Asp362 in Drosophila) is shown in the orange box and the Pro308 residue is shown in the pink box.
4 Figure S2 A Control 100 na SYT #1 SYT #2 B eejc Amplitude (na) **** C 0.2 mm 20 ms 10 ms D Rise Time (ms) Control SYT #1 SYT #2 **** *** SYT #1 SYT #2 E F 2 mm 10 ms Rise Time (ms) **** **** * SYT #1 SYT #2
5 Figure S2. Effects of DSYT1 on synaptic transmission in 0.2 and 2.0 mm extracellular calcium. (A) Representative EPSCs recorded in 2.0 mm extracellular calcium at third instar larval muscle 6 synapses for the indicated genotypes (control, or DSYT1 in transgenic lines #1 and #2 induced by elav C155 GAL4). Similar to the effects at 0.2 mm calcium, reduces evoked release. (B) Quantification of mean eejc amplitudes in the indicated genotypes (w /, 303.4±26.4 na, n=8; elav C155 GAL4; UAS DSYT1, 260.5±15.7 na, n=13; elav C155 GAL4; UASDSYT1 #1, 115.1±13.1 na, n=13; elav C155 GAL4; UASDSYT1 #2, 114.9±15.7 na, n=17). (C) Average traces of EPSCs normalized to the maximal amplitude following induction of WT DSYT1 (blue), DSYT1#1 (green) or DSYT1#2 (magenta) by elav C155 GAL4 in 0.2 mm external calcium. (D) Quantification of average rise time in each genotype. The induction of in transgenic line #2 results in slower kinetics of neurotransmitter release compared to control. Mean rise times at 0.2 mm calcium are: WT DSYT1, 1.15 ± 0.04 ms, n=15; DSYT1#1, 1.27 ± 0.06 ms, n=16; DSYT1#2, 1.77 ± 0.12 ms, n=16. Student s ttest revealed significant differences between WT DSYT1 and DSYT1#2 (P<0.0002) and DSYT1#1 and DSYT1#2 (P<0.002). (E) Average traces of EPSCs normalized to the maximal amplitude following induction of WT DSYT1 (blue), DSYT1#1 (green) or DSYT1#2 (magenta) by elav C155 GAL4 in 2.0 mm external calcium. In higher calcium, both lines have slower rates of release than controls. (F) Quantification of average rise time in each genotype. Mean rise times at 2 mm calcium are: WT DSYT1, 0.7 ± 0.03 ms, n=13; DSYT1#1, 1.0 ± 0.05 ms, n=13; DSYT1#2, 1.2 ± 0.06 ms, n=17. Student s ttest revealed significant differences between WT DSYT1 and DSYT1#1 (P<0.001),
6 WT DSYT1 and DSYT1#2 (P<0.001) and DSYT1#1 and DSYT1#2 (P<0.02).
7 Figure S3 A 0.2 mm B C E Norm. Cum. Release Norm. Cum. Release Time (ms) 2 mm Time (ms) 0.2 mm D Release Time (ms) (90% of total release) Release Time (ms) (90% of total release) F **** *** SYT #1 SYT #2 **** SYT #1 SYT #2 2 mm 100 na SYT #1 50 na 10 ms SYT #1 10 ms SYT #2 SYT #2 G 0.2 mm H mm (It / I1) 1.5 (It /I1) Stimulus # Stimulus #
8 Figure S3. Effects of DSYT1 on synaptic transmission kinetics and high frequency stimulation. (A) Cumulative response normalized for the maximum following induction of WT DSYT1 (blue), DSYT1#1 (green) or DSYT1#2 (magenta) by elav C155 GAL4 in 0.2 mm external calcium. Dash lines indicate the time at which 90% of the total release has occurred during a single stimulus. Induction of in the transgenic line #2 results in slower rates of release due to an enhancement in the slower asynchronous phase of fusion. (B) Quantification of release time when 90% of the total charge was transferred in each condition. Mean release time in the strains at 0.2 mm calcium are: WT DSYT1, 14.4 ± 0.8 ms, n=15; DSYT1#1, 15.9 ± 0.9 ms, n=16; DSYT1#2, 21.6 ± 1.4 ms, n=16. Student s ttest revealed significant differences between WT DSYT1 and DSYT1#2 (P<0.0001) and DSYT1#1 and DSYT1#2 (P<0.005). (C) Cumulative release normalized for the maximum following induction of WT DSYT1 (blue), DSYT1#1 (green) or DSYT1#2 (magenta) by elav C155 GAL4 in 2.0 mm external calcium. Dash lines indicate the time at which 90% of the total release has occurred during a single stimulus. (D) Mean release time at 2 mm calcium: WT DSYT1, 8.6 ± 0.4 ms, n=11; DSYT1#1, 10.0 ± 0.8 ms, n=13; DSYT1#2, 11.6 ± 0.7 ms, n=17. Student s ttest revealed significant differences between WT DSYT1 and DSYT1#1 (P<0.001). (E, F) Representative EPSCs following induction of WT DSYT1 (blue), DSYT1#1 (green) or DSYT1#2 (magenta) by elav C155 GAL4 in 0.2 mm (E) or 2.0 mm (F) external calcium during 10 Hz tetanic stimulation of the nerve. (G, H) Average responses for 500 stimulations normalized to the first response during the tetanus following induction of WT DSYT1 (blue), DSYT1#1 (green) or DSYT1#2 (magenta) by elav C155 GAL4 in 0.2 mm (G) or 2.0 mm (H)
9 extracellular calcium. DSYT1 decreases initial release probability and results in facilitation in low calcium (G) or slower rates of depression in high calcium (H).
10 Table S1. Electrophysiologic Data (USA1) Characteristic I.2 II.2 III.1 III.2 Ulnar motor nerve Pre exercise CMAP amp. (mv) Post exercise CMAP amp. (mv) Median motor nerve Pre exercise CMAP amp. (mv) Post exercise CMAP amp. (mv) Peroneal motor nerve (TA) Pre exercise CMAP amp. (mv) Post exercise CMAP amp. (mv) Peroneal motor nerve (EDB) Distal CMAP amp. (mv) Tibial motor nerve Distal CMAP amp. (mv) Ulnar sensory nerve Amp. ( V) Sural sensory nerve Amp. ( V) Ulnar motor nerve 3Hz RNS (% decrement) Baseline Immed. post exercise % Amp. Amplitude; CMAP Distal compound muscle action potential; CV conduction velocity; TA tibialis anterior muscle; EDB extensor digitorum brevis muscle; RNS repetitive nerve stimulation; not tested 10% 0% % % 8%
11 Table S2. Electrophysiologic Data (UK1) Characteristic II.2 III.2 III.7 Ulnar motor nerve Pre exercise CMAP amp. (mv) Post exercise CMAP amp. (mv) Median motor nerve Pre exercise CMAP amp. (mv) Post exercise CMAP amp. (mv) Peroneal motor nerve (TA) R L Pre exercise CMAP amp. (mv) Post exercise CMAP amp. (mv) Peroneal motor nerve (EDB) Distal CMAP amp. (mv) Tibial motor nerve Distal CMAP amp. (mv) Ulnar sensory nerve a Amp. (µv) CV(m/s) Sural sensory nerve Amp. (µv) Median motor nerve 3Hz RNS (% decrement) Baseline 2% 3% 0% Amp. Amplitude; CMAP Distal compound muscle action potential; CV conduction velocity; TA tibialis anterior muscle; EDB extensor digitorum brevis muscle; RNS repetitive nerve stimulation; a orthodromic stimulation; not tested
12 Table S3. Whole Exome sequencing in USA1 and UK1: Variants Segregating under an Autosomal Dominant Model with strict filtering and Conservation Criteria. 3a. USA1 Family CHROMOSOME POSITION ALLELE GENE AMINO ACID SCORE CHANGE NAME CHANGE A>C SYT2 a Asp307Ala C>G THADA Gly182Ala C>T ASTL Val166Ile G>G EYA1 a Pro84Leu T>C SLC27A4 Met266Thr T>C PSMA4 Met72Thr 3 3b. UK1 Family CHROMOSOME POSITION ALLELE GENE AMINO ACID SCORE CHANGE NAME CHANGE C>T SYT2 a Pro308Leu T>G ECEL1 His412Pro C>A NPAS3 Asp438Glu 3 SCORE: This is the composite of 5 protein prediction algorithms where damaging earns one point (Polyphen, Mutation Taster, Mutation Assessor, SIFT, LRT). a Variants segregating with disease following Sanger sequencing of all identified genes in USA1 and UK1 families.
13 Supplemental Reference 1. Fernandez, I., Araç, D., Ubach, J., Gerber, S.H., Shin, O., Gao, Y., Anderson, R.G., Südhof, T.C., Rizo, J. (2001). Threedimensional structure of the synaptotagmin 1 C2Bdomain: synaptotagmin 1 as a phospholipid binding machine. Neuron 32, (2001).
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