Del Viso F , Huang F , Myers J , Chalfant M , Zhang Y , Reza N , Bewersdorf J , Lusk CP , Khokha MK .

R01 HL124402 NHLBI NIH HHS , T32 GM007223 NIGMS NIH HHS , P30 DK045735 NIDDK NIH HHS , S10 OD020142 NIH HHS , UL1 TR001863 NCATS NIH HHS , Wellcome Trust , 095927/A/11/Z Wellcome Trust , 203285/Z/16/Z Wellcome Trust

             determination of left/right symmetry
             motile cilium assembly
             nuclear pore inner ring
             pore complex
             nuclear pore complex assembly
             determination of heart left/right asymmetry

                congenital heart disease

Xtr Wt + nup188 (Fig. S 2 A)
Xtr Wt + nup188 (Fig. S 2 B C)
Xtr Wt + nup188 (Fig. S 2 B C)
Xtr Wt + nup188 (Fig. S 2 D)
Xtr Wt + nup188 MO (Fig. 1 B C)
Xtr Wt + nup188 MO (Fig. 1 B C)
Xtr Wt + nup188 MO (Fig 1. B C)
Xtr Wt + nup188 MO (Fig. 1 D E)
Xtr Wt + nup188 MO (Fig. 1 D E)
Xtr Wt + nup188 MO (Fig. 1 D E)
Xtr Wt + nup188 MO (Fig. 1 F G)
Xtr Wt + nup188 MO (Fig. 1 F H)
Xtr Wt + nup188 MO (Fig. 2 A B)
Xtr Wt + nup188 MO (Fig. 2 A B)
Xtr Wt + nup188 MO (Fig. 2 A B)
Xtr Wt + nup188 MO (Fig. 3 A left)
Xtr Wt + nup93 MO (Fig. 1 B C)
Xtr Wt + nup93 MO (Fig. 1 D E)
Xtr Wt + nup93 MO (Fig. 1 F G)
Xtr Wt + nup93 MO (Fig. 1 F H)
Xtr Wt + nup93 MO (Fig. 2 A B)
Xtr Wt + nup93 MO (Fig. 2 A B)
Xtr Wt + nup93 MO (Fig. 2 A B)
Xtr Wt + nup93 MO (Fig. 3 A right)
Xtr Wt + nup93 MO (Fig. S 1 D-F)
Xtr Wt + nup93 MO (Fig. S 1 G)

	Figure 1. Depletion of Inner-Ring Nups Alters LR Patterning (A) One- (left) and 2-cell (right) injection schematic (not to scale) showing a salmon-colored dye as a tracer. When injections are done in one cell at the 2-cell stage, embryos are selected where either the left or the right side of the embryo is targeted, as shown in the diagram of dissected LRO (stage 16) or in a later stage-27 embryo. Small red lines in LRO represent cilia. (B) Percentage of embryos with abnormal cardiac looping (see C for key to score cardiac looping) after MO injection at 1-cell stage (left) or 2-cell stage (right). nup188 morphant heart looping defects are rescued by human NUP188 expression (left). n represents total number of embryos from three independent experiments. ∗∗∗p < 0.0005, ∗∗p < 0.005, chi-squared/Fisher's exact test. UC, uninjected controls. (C) Examples of cardiac looping phenotypes of wild-type and abnormal Xenopus hearts at stage 45 viewed ventrally with anterior at the top. D-Loop: normal outflow track (OT) loops right (short dashed line). L-Loop: abnormal OT loops left. A-Loop: abnormal OT is unlooped. Ventricle (V) is bound by a long dashed line. (D) Percentage of embryos with abnormal pitx2c (see E for key to score pitx2c staining) after MO injection at 1-cell stage (left, middle) or 2-cell stage (right). n represents total number of embryos from three independent experiments. ∗∗∗p < 0.0005, ∗p < 0.05, chi-squared/Fisher's exact test. (E) Example key of pitx2c expression showing lateral views of embryos (stages 28–31) with dorsal at the top. Arrowheads point to pitx2c in the lateral plate mesoderm. (F) Percentage of embryos with abnormal coco expression (see G for key for coco scoring) after MO injection at 1-cell stage (left, middle) or 2-cell stage (right). L and R denote left and right side of LRO, respectively. n represents total number of embryos from three independent experiments. ∗∗∗p < 0.0005, ∗∗p < 0.005, chi-squared/Fisher's exact test. (G) Example key of coco expression patterns in the LRO at stages 19–20. Ventral views with anterior at the top. (H) Schematic of NPC. Nups referred to in this study are in bold. (I) Nup188 and Nup93 protein levels determined by western blot. Numbers are relative protein levels normalized to Gapdh with triangle reflecting dose of MO. Boxed lane indicates dose used for all experiments. See also Figures S1 and S2.
	Figure 2. nup188 and nup93 Depletion Decreases Cilia in the LRO (A) LROs from embryos treated with the indicated MOs (or UC) stained with anti-acetylated α-tubulin (α-AcTub, green) to detect primary cilia, Phalloidin (red) marks the cell borders. p, a, l, and r denote posterior, anterior, left, and right, respectively. Right panels show a magnification of a representative region of the LRO. (B) Box plots of cilia number per LRO area (μm2) of embryos derived from injections at the 1- or 2-cell stage. Box depicts 25th to 75th percentiles with median marked by a horizontal line in the box. Whiskers indicate data range from smallest to largest values. n represents total number of embryos from three independent experiments. ∗∗∗p < 0.0005, ∗∗p < 0.005, Student’s t test.
	Figure 3. Depletion of Nup93/188 Affects Cilia but Not NPCs (A) Fluorescence images of lateral views, with dorsal at the top, of both sides (uninjected and injected) of a single embryo with the cilia of the multiciliated cells (MCCs) labeled with α-AcTub (green). Nuclei stained with Hoechst (blue). Insets (top right) are a magnification of a cluster of MCCs (scale bar, 20 μm). The disruption of cilia was found in 100% (n = 73) of nup93 morphants and in 41% (n = 70) of nup188 morphants. (B) Fluorescence images of Xenopus embryos injected with nup62 (n = 30) or nup133 (n = 33) MOs at the 1-cell stage labeled with anti-AcTub (green). Lateral views of embryos, with dorsal at the top (top panels) and higher magnification of the MCCs in the bottom panels. Nuclei stained with Hoechst (blue). Level of nup depletion in these morphants is shown in Figure S1A. (C) Embryos were co-injected with mRNA encoding NLS-GFP and nup93, nup188, or nup133 MOs. Animal caps were dissected and allowed to develop MCCs before imaging the distribution of NLS-GFP. Cilia in these explants are shown in Figure S1J. (D) Staining of NPCs with the mAb414 antibody in animal caps of UC and embryos injected with the indicated MOs. (E) Graph shows the mean nuclear/cytoplasm (N:C) fluorescence ratios of NLS-GFP with SD; n represents total number of nuclei from three independent experiments. ∗∗∗p < 0.0005, Student’s t test. (F) Graph shows the mean and SD of the NPC density in animal caps of UCs and embryos injected with the indicated MOs. n represents number of nuclei from three independent experiments. See also Figures S1 and S2.
	Figure 4. Nup188 and Nup93 Specifically Localize to the Bases of Cilia (A) Immunofluorescence images of Xenopus epidermal MCCs stained with anti-Nup93 (green) and either anti-AcTub (red, top) or anti-γTub (red, bottom) antibodies with merge. (B) Immunofluorescence images of human RPE cells stained with the indicated anti-nup antibodies (left) with anti-AcTub, anti-γTub, or anti-Cep290 (middle) and merge (right). See Figure S3B for location of cilia-specific epitopes. (C) Anti-Nup93 antibodies are specific. Fluorescence image (merge of green and red channels) of representative scrambled (mock) siRNA-treated RPE cell stained with anti-Nup93 (green) and anti-AcTub (red) antibodies. Panels on right are higher magnification of cilium base showing just the anti-Nup93 signal (green; top) and merge of anti-Nup93 and anti-AcTub (red) images (bottom). Arrowhead points to cilium base. N denotes the nucleus. (D) Identical to (C) except that cells are treated with siRNAs specific to NUP93 (N93). (E) Plot of normalized fluorescence intensity in a.u. of anti-Nup93 signal at cilium base and NPCs of individual cells treated with scrambled (mock) or specific NUP93 (N93) siRNAs. Mean ± SD is indicated; n represents total number of cells/cilia from three independent experiments. ∗∗∗p < 0.0005, Student’s t test. (F) Western blot of Nup93 levels after siRNA transfection; numbers are quantification of protein levels relative to Gapdh. (G–J) Anti-Nup188 antibodies are specific. Panel layout is identical to (C)–(F) except that cells are treated with scrambled (mock) or siRNAs specific to NUP188 (N188). (K) Plot of percentage of cells in which the anti-nup signal co-localizes with a cilium-base marker. Mean ± SD is indicated; n represents total number of cells from three independent experiments. See also Figures S1 and S3.
	Figure 5. Nups Do Not Form NPC-like Rings at Cilia Bases (A) 2D FPALM super-resolution image of a cell co-stained with anti-Nup93 (red; AF647) and anti-AcTub antibodies (green; Cy3B). (B) Higher-magnification views of the nuclear surface (left panels) and the cilium base (right panels) of two different cells stained with anti-Nup93 (AF647). (C) Box plot where the density of localization clusters at the nuclear envelope and cilia bases are directly compared. The box depicts the 25th to 75th percentiles with the median marked as a horizontal line in the box. The whiskers mark the data range from the smallest to the largest value. “+” indicates the mean of the distribution (n represents number of cells). ∗∗p < 0.005, Student’s t test. (D) Plot of the diameter (mean ± SD) of localization clusters at the nuclear envelope and cilia bases. n represents number of localization clusters from three independent experiments. ∗∗∗p < 0.0005, Student’s t test. (E) 2D FPALM images of anti-Nup188 (red; AF647) and anti-γTub antibodies (green; Cy3B) with merge on right. (F) As in (E) except with anti-AcTub co-stain. (G) STED images of a cell co-stained with anti-Nup188 (red; ATTO647N) and anti-γTub antibodies (green; ATTO594) with merge on right. (H) As in (G) except with anti-AcTub co-stain. See also Figure S4.
	Figure S1 (related to Figures 1,2,3 and 4): Nup188 and Nup93 are required for cilia in mammalian cells and Xenopus. (A) Nup62 and Nup133 protein levels after MO injection. Western blots of Nup62 and Nup133 in both uninjected controls (UCs) and embryos injected with nup62 and nup133 MOs (nup62 MO doses: 5 and 10ng/embryo) (nup133 MO doses: 2.5, 5 and 10ng/embryo). Numbers above each lane indicate the band intensity normalized to Gapdh (loading control). Boxed lanes indicate the dose used in epidermal cilia stain in Figure 3B. (B) Nup188 is required for cilia in human RPE cells. Merged (green and blue channels) fluorescent images of human RPE cells induced to ciliate after knockdown of Nup188 or Nup93 using specific siRNAs or scrambled (mock) control. Cilia are stained with an Arl13b antibody (green) and DNA with Hoechst (blue). See also Figure 4F and 4J for degree of knockdown. (C) Nup188 depletion in RPE cells leads to decreased ciliation. Plot of percentage of ciliated cells after knockdown of Nup188 or Nup93 using specific siRNAs in human RPE cells. n=total number of nuclei/cilia from 3 independent experiments. Chi-Square Test, *** p<0.0005. (D-F) Loss of nup93 affects gliding in Xenopus embryos. (D) At stages 28-31, wildtype embryos glide along the surface of an agarose-coated dish due to the beating of multiciliated cells while nup93 morphants do not. Brightfield images of 2 UCs (top) and 4 nup93 morphant embryos (bottom). (E) Same field as (D) but nup93 morphants are identified by Alexa488 tracer dye (bottom 4 green morphants). (F) Video frame captures of the same UC and morphant embryos in (D) and (E) gliding at indicated times. See also Movie S1. (G) Nup93 is specifically required for epidermal cilia. Plot of the percentage of embryos with abnormal epidermal cilia assessed by anti-AcTub staining after injection at 1-cell stage with nup93 MO (1 ng/embryo) or (to assess specificity) with nup93 MO combined with human (h) NUP93 mRNA (50 or 100 pg/embryo). Bottom panel is a key (blue, green, orange, red) to our qualitative assessment of cilia shown as example fluorescent images of embryos (lateral views, dorsal at top) stained with anti-Actub (green) and Hoechst (blue). n=total number of embryos from 3 independent experiments, Chi-Square Test, *** p<0.0005. (H-I) Cilia loss in nup morphants is not due to changes in cilia cell type specification. (H) In situ hybridizations images with a foxj1-specific probe of stage 10.5 embryos injected with the indicated MOs or with Xtnup188 mRNA. Vegetal views of embryos with blastopore lip to the top are shown as representative examples of 2 independent experiments. Numbers indicate the number of embryos showing the same staining pattern. (I) In situ hybridizations images with a foxj1-specific probe of stage 28-31 embryos injected with the indicated MOs. Left, lateral views of embryos with dorsal at the top are shown as representative examples of 3 independent experiments. (J) Nup188 and Nup93 depletion affects multiciliated cells in Xenopus epidermis. Fluorescent images of epidermal animal caps derived from UC embryos or those injected with the indicated MOs; multiciliated cells (MCCs) labeled with anti-AcTub (green). Two z-sections (top and bottom panels) at the indicated focal planes are shown
	Figure S2 (related to Figures 1, 2 and 3): Nup188 overexpression specifically affects cardiac looping and cilia. (A) Overexpression of Nup188 affects heart looping. To drive overexpression of Nup188, Xenopus tropicalis (Xt) nup188 mRNA or human (h) NUP188 mRNA were injected at 1-cell stage. Plot shows the percentage of resulting embryos with cardiac looping defects. Chi-Square or Fisher’s Exact Test, ***p<0.0005, **p<0.05. n=total number of embryos from 3 independent experiments. (B) LROs from control embryos (UC) and embryos injected with the Xtnup188 mRNA at the 1 or 2-cell stage. Primary cilia were stained with anti-AcTub (-AcTub, green). Phalloidin was used to mark cell borders (red). Xtnup188 mRNA was traced using an mRNA encoding for a GFP-tagged plasma membrane protein (magenta). p,a,l,r: posterior, anterior, left, right, respectively. (C) Box plots show cilia number per LRO area (µm2) of UC and embryos injected at the 1 or 2-cell stage with Xtnup188 mRNA. The box depicts the 25th to 75th percentiles with the median marked as a horizontal line. The whiskers mark the data range from the smallest to the largest value. In embryos injected at the 2-cell stage, blue boxes are the uninjected side and red boxes the injected side. n=total number of embryos from 2 independent experiments, T-test, *** p<0.0005, * p<0.05. (D) Xenopus embryos were injected with Xtnup188 mRNA into 2-cell stage such that half the embryo receives the mRNA (See Figure 1A for a visual guide to these experiments). Fluorescence images are lateral views, with dorsal at the top, of both sides (uninjected and injected) of a single embryo with the cilia of the MCCs labeled with anti-AcTub (green). Nuclei stained with Hoechst (blue). The disruption of cilia on the injected side was found in 35% (n=70) of embryos from 2 independent experiments. (E) Fluorescent images of NPCs stained with the mAb414 antibody in animal caps of UC and embryos injected with Xtnup188 mRNA. (F) Fluorescent images of embryos co-injected with mRNA encoding NLS-GFP and Xtnup188 mRNA. Animal caps were dissected and allowed to develop MCCs before imaging. (G) Embryos were co-injected with mRNA encoding NLS-GFP and Xtnup188 mRNA. Graph shows the nuclear/cytoplasm (N:C) ratio of mean NLS-GFP fluorescence intensities and the SD. n=total number of nuclei from 3 independent experiments.
	Figure S3 (related to Figure 4): Nup93/188 localize to the mother and daughter centriole. (A) An overexpressed SNAP-Nup188 co-localizes with centrioles. Fluorescent micrographs of HeLa cells expressing SNAP-Nup188 detected with the oregon-green SNAP substrate. Centrioles were detected with an anti-Cep152 antibody (red) and DNA stained with Hoechst (blue) in merge panel. (B) Schematic of the cilium. BB is basal body (mother centriole), DC is daughter centriole and TZ is transition zone. (C) Nup93 localizes to the BB and DC. Deconvolved fluorescent micrographs of the bases of cilia in RPE cells immunostained with the indicated anti-Nup93 antibodies (green) and those that stain different components of the cilium base (red). Pixels under the white line in merged image were used to generate line profile plots in right panels. (D) Nup188 localizes to the BB and DC. Deconvolved fluorescent micrographs of the bases of cilia in RPE cells immunostained with the indicated anti-Nup188 antibodies (green) and those that stain different components of the cilium base (red). Pixels under the white line in merged image were used to generate line profile plots in right panels.
	Figure S4 (related to Figure 5): Comparison of number of detections per cluster for both Nup93 and Nup188 in 2D-FPALM and fluorescence intensity in STED. (A) Two-color 2D-FPALM image of cell labeled with anti-AcTub (green) and anti-Nup93 (red). Three boxed ROIs from the nuclear surface, the cilium base, and the cellular background are magnified in B-D. (B-D) Magnification of the three ROIs shown in panel A showing number of localizations for a selected number of clusters (white boxes) in all three ROIs. (E) STED images of immunolabeled anti-Nup188 clusters at the cilium base. ROIs are selected from both the cilium base and the cellular background to show the increased fluorescence intensity (in arbitrary units) of clusters at the basal body (far right panels, white boxes). Diffraction limited confocal images are also shown in middle panels.
	Figure S5 (related to Figure 6): Nup188 is found in multiple copies within evenly spaced clusters at the cilium base. (A) The number of anti-Nup188 localizations (detections) per cluster from 10 W-4PiSMSN images of cilia bases (left) and corresponding randomly selected regions (right). (B) Cumulative density distribution of data shown in A for better visualization of histograms. (C) Nearest neighbor distance distribution between the cilia bases (left; reproduced from Figure 6B) and randomly selected locations from 17 images (right). a.u. is arbitrary units.
	Figure S6 (related to Figure 6 and movie S3): Distribution of anti-Nup188 single molecule detections with reference to cylinder surface. Distribution of the distances of single molecule detections of 5 cylinder-modeled Nup188 structures (see Movie S3) showing a compact distribution around the cylindrical surface. Negative values indicate the detections are within the cylinder and positive values are outside.
	Figure 6. Nup188 Forms Two Barrel-like Structures that Encase the Centrioles (A) Diffraction-limited (inset) and 3D W-4PiSMSN super-resolution image of anti-Nup188 signal at the cilium base. Heatmap coloration reflects depth in z as depicted by scale. Individual structures are circled. See also Movie S2. (B) Nearest-neighbor distances from all localiza- tion clusters in all structures imaged were calcu- lated and plotted. (C–E) Rotated views of image in (A) where two cylinders (blue and red) have been fitted into both structures denoted by ‘‘1’’ and ‘‘2.’’ See also Movie S2. (F–I) Planar sections of each structure cut across the cylinder axis (central point). Dotted lines represent cylinders. (J and K) Distribution of the distances of individual localizations from W-4PiSMSN data inside (nega- tive values) and outside (positive values) the modeled cylinder surface of structure 1 (J) and structure 2 (K). (L) QR code to load Nup188 W-4PiSMSN structure into the 3D visualization application Augment. See Experimental Procedures for instructions. See also Figures S5 and S6.

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