Nature Neuroscience: doi: /nn.2662
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1 Supplementary Figure 1 Atlastin phylogeny and homology. (a) Maximum likelihood phylogenetic tree based on 18 Atlastin-1 sequences using the program Quicktree. Numbers at internal nodes correspond to bootstrap support values. (b) Sequence alignment of human and zebrafish Atlastin-1 homologues. Black letters on a grey background represent residues that are identical between orthologous sequences while + symbol indicates amino-acids that are similar. Atlastin functional domains are underlined in red for the GTPase domain, including the three GTP-binding sites that are boxed, and in green for the two transmembrane domains. (c) Surrounding synteny of the atl1 gene in the zebrafish, mouse and human genomes. atl1, highlighted in green, is surrounded by the same genes, Map4k5 and Sav1, in all three genomes, showing a strong conservation of this genomic area. These three genes are only found in one copy in the zebrafish genome, indicating that the teleost duplication of this region has been lost in the zebrafish.
2 Supplementary Figure 2 Full-length western blots of Figures 1b-c and 6a. Red boxes indicate the cropped regions shown in Figures 1b-c and 6a. (a) Atlastin expression during zebrafish development. (b) Analysis of atl1 knockdown efficiency. (c) Increased phosphorylation of Smad1/5/8 in 24-hpf atl1 morphants (MO atl ). Western blot analyses showing the differential levels of Atlastin, phosphorylated Smad1/5/8 (P-Smad1/5/8) and type I BMP receptor (BMPRI) between 24-hpf control and MO atl embryo. All the samples derive from the same set of injected embryos and blots were processed in parallel.
3 Supplementary Figure 3 Abnormal architecture of spinal primary and secondary motor axons in atlastin (atl1) morphants. (a) Analyses of neuromuscular synapse formation in 24- and 56-hpf control and atl1 morphant (MO atl ) by doubly labeling spinal motor neurons with znp-1 (green) and AChR clusters with Alexa Fluor 555-abungarotoxin (red). Lateral views of the trunk, anterior to the left. In contrast to controls, 24-hpf MO atl primary motor neurons display abnormal branching (arrows) and form fewer synapses (asterisks) as revealed by the merge pictures. At 56-hpf, MO atl spinal motor neurons show numerous ectopic branches which form aberrant synapses with lateral myotome (arrows) compared to control spinal motor neurons. (b) Immunolabeling of secondary motor neurons in 56-hpf control and atl1 morphant embryos using zn-5 antibody. Right panels represent higher magnifications of left panels. MO atl secondary motor neurons fail to grow rostrally (thin arrows; n=27/30 larvae) compared to control motor neurons (arrowheads). Spinal motor tracts appear abnormally defasciculated at the horizontal myoseptum (asterisks) in 64% of morphant larvae (n=19/30) compared with control larvae. In addition, some MO atl secondary motor neurons show ectopic exit point from the spinal cord (thick arrow; n=9/30). Scale bars, 20 m.
4 Supplementary Figure 4 Aberrant distribution of neurons in atlastin (atl1) morphant hindbrain and spinal cord. (a-d) Immunolabeling of post-mitotic neurons with HuC/D antibody in 22-hpf control (a,c) and atl1 morphant (MO atl ; b,d) embryos. Scale bars, 50 m. (a-b) Dorsal view of flat-mounted control and MO atl hindbrains, anterior to the left. Arrow indicates position abnormality along the MO atl hindbrain midline. (c-d) Lateral view of control and MO atl spinal cords, anterior to the left/bottom. (c) Short arrows mark the stereotypical organization of primary motor neurons in control spinal cords. (d) Long arrow indicates impaired distribution of MO atl spinal motor neurons. (c-d) Insets show cross-section of 22-hpf control and MO atl spinal cords labeled by in situ hybridization using an Olig2 RNA probe, marking the entire motor neuron domain (pmn).
5 Supplementary Figure 5 Analysis of cell death and proliferation in atlastin (atl1) morphant embryos. (a-b) Dorsal views of the hindbrain (top panels) and lateral views of the trunk (bottom panels), anterior to the left. Scale bars, 100 m. (a) Whole-mount co-immunolabelling of 22-hpf control and atl1 morphant (MO atl ) embryos using the pan-neural anti-huc/d (green) and anti-activated-caspase 3 (red) antibodies. No significant differences in the accumulation of apoptotic neurons were observed in MO atl hindbrain and spinal cord compared to controls. (b) Immunodetection of 22-hpf control and MO atl embryos with Phospho-histone H3 (H3P) antibody, a marker of mitotic cells. Cell proliferation does not significantly vary between control and morphant embryos.
6 Supplementary Figure 6 Normal development of branchiomotor and sensory Rohon- Beard neurons in atlastin (atl1) morphant embryos. (a) Immunodetection of 56-hpf non-injected and atl1 morphant (MO atl ) Islet1:GFP transgenic embryos using anti-gfp antibody. Dorsal views of the hindbrain on the top panels, anterior to the top. Lateral view of the hindbrain on the bottom panels, anterior to the left. Branchiomotor neurons do not show any obvious defects of positioning and axon pathfinding in MO atl larvae. (b) Whole-mount immunolabeling of control and MO atl sensory Rohon-beard neurons with zn-12 antibody at 24-hpf. Lateral views of the trunk, anterior to the left. The positioning and number of Rohon-Beard neurons appear unchanged by atl1 knockdown. Scale bars, 100 m.
7 Supplementary Figure 7 atlastin (atl1) knockdown and overexpression modulate the level of phosphorylated Smad. (a) Western blot analyses of the level of phosphorylated Smad1/5/8 (P-Smad1/5/8) from control (Ctl) and atl1 morphant (MO atl ) protein extracts at different developmental stages. H2b was used as a loading control. Until tailbud stage, P-Smad1/5/8 level does not vary between control and morphant embryos whereas it appears significantly increased in MO atl embryos from the 18-somite stage onwards. (b) Western blot and quantification analyses of P-Smad1/5/8 level in total protein extracts from 24-hpf control (Ctl), atl1 morphant (MO atl ), mrna-injected (mrna atl ) and rescued (MO atl + mrna atl ) embryos. H2b was used as a loading control. Bottom histogram represents the quantification of P-Smad1/5/8 immunoblot band intensity normalized to the H2b value in three independent experiments. A total of 30 embryos from each set were used in each experiment; atl1 knockdown significantly increases P-Smad1/5/8 level (p=0.002) whereas atl1 overexpression decreases it (p=0,04). Rescued embryos, concomitantly injected with atl1 MO and mrna, show a similar P-Smad1/5/8 level as control embryos (p=0,636). Error bars are SE. P-values were calculated using a Student s unpaired t test.
8 Supplementary Figure 8 Atlastin co-localizes with endosomal markers in zebrafish spinal neurons. (a-c) Immunolabeling of zebrafish cultured spinal neurons at 28 hours post-plating. Arrows indicate the region of the axon magnified in the inset. Images, and thereby neuron cell bodies, are voluntarily overexposed to detect signals in the axons and focus on axonal co-localization. (a) Co-immunostaining of Atlastin and -Tubulin. Insets illustrate Atlastin enrichment at spinal neuron growth cones. (b) Coimmunodetection of Atlastin and Rab5a demonstrating that Atlastin is partially located in early endosomes (n=100 neurons). (c) Co-immunostaining of Atlastin and the late endosome marker Rab7, indicating that Atlastin is also present in late endosomes (n=100 neurons). Scale bars, 10µm.
9 Supplementary Figure 9 Subcellular distribution and morphology of early and late endosomes in primary cultures of spinal neurons from control and atlastin morphant (MO atl ) embryos. Immunolabeling of Rab7, a late endosomal marker (top panels), and Rab5a, an early endosomal marker (bottom panels) in 19-hour post-plating primary cultures of spinal neurons derived from 18-somite control and MO atl embryos. Left panels show spinal neurons and right panels illustrate non-neuronal cells. No significant differences in late and early endosomes were revealed between control and morphant primary cultures (n=100 neurons analyzed in each set of cultures). Scale bar, 20µm.
10 Supplementary Figure 10 Morphological analysis of the endoplasmic reticulum (ER) in primary cultures of spinal neurons derived from control, atl1 morphant (MO atl ) and atl1-overexpressing (WT + mrna atl ) embryos. Co-immunolabeling of the ER marker calreticulin and the spinal motor neuron marker znp1, in 19-hour post-plating primary cultures of spinal neurons derived from 18-somite control, MO atl and (WT + mrna atl ) embryos. Left and middle panels show spinal motor neurons and right panels show fibroblasts. Insets represent higher magnifications. ER morphology appears unchanged in MO atl and atl1-overexpressing spinal neurons and fibroblasts compared to control cells (n=100 neurons and n=100 fibroblasts analyzed in each set of cell cultures). Scale bars, 10µm.
11 Experiment 1 Experiment 2 Experiment 3 Experiment 4 Transplant type Number of wt embryos transplanted Selected healthy embryos showing GFP innervation in 14 somites Number of embryos with impaired motility Hb9-GFP>WT 31 12/31 0/12 Hb9-GFP;MO atl >WT 39 18/39 13/18 Hb9-GFP>WT 28 15/28 0/15 Hb9-GFP;MO atl >WT 33 14/33 14/14 Hb9-GFP>WT 28 17/28 1/17 Hb9-GFP;MO atl >WT 27 16/27 14/16 Hb9-GFP>WT 31 14/31 0/14 Hb9-GFP;MO atl >WT 44 29/44 21/29 Supplementary Table 1 Number of successful transplants and impact of the transplant upon motility at day 4. Hb9GFP stands for Tg(mnx1:mGFP) transgenic embryos. An average of cells have been transplanted into wild-type dorsoposterior epiblast (location of ventral spinal cord precursors) at 70-80% epiboly. Successful transplants (i.e., containing GFP + innervation in at least 14 somites) also show some notochord and somatic donor cells (evaluated by dextran detection, data not shown).
12 Embryos Treatment Number Normal mobility Swimming deficit Mild Severe Control none % / / Control DMSO % / / Control Dorsomorphin % / / MO atl none 71 12% 17% 71% MO atl DMSO 65 11% 20% 69% MO atl Dorsomorphin 77 67% 30% 3% Supplementary Table 2 A treatment with BMP-inhibiting dorsomorphin rescues the morphant larval mobility. MO atl = atlastin morphants; 25 µm Dorsomorphin and DMSO were added to E3 medium at the 16-somite stage. Mild and severe swimming deficits were assessed using a touch-response test at 72 hpf. Mildly affected larvae respond to touch and swim over a short distance of 2-3 cm, while severely affected larvae only respond to touch after several stimuli and either move significantly more slowly over a distance < 2 cm or coil but do not swim.
13 Supplementary Video Legends Supplementary Video 1 Abnormal touch-evoked motility of atlastin (atl1) morphant larvae. Touch-response mobility of 72-hpf (a) control larvae, (b) atl1 morphant larvae and (c) rescued larvae co-injected with atl1 MO and human ATL1 transcript. Supplementary Video 2 The motility deficit of atlastin (atl1) morphant larvae is tightly correlated with abnormal branching of spinal motor axons. Touch-response mobility of 4-dpf (a) control (Hb9:GFP; WT), (b) atl1 morphant (Hb9:GFP; MO atl ) and (c) transplanted (Hb9:GFP; MO atl >WT) mosaic larvae. Supplementary Video 3 The swimming deficit of atlastin (atl1) morphants is rescued by genetic inhibition of BMP signaling. Touch-response mobility of 72-hpf (a) heatshocked and non-injected Tg(hs:DN-BMPRI) transgenic larvae, (b) atl1 morphant Tg(hs:DN-BMPRI) larvae which were not submitted to heat shock and (c) MO atl /Tg(hs:DN-BMPRI) that were heat-shocked at hpf and therefore expressed a dominant-negative version of type-i BMP receptor.
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