Corradi E , Dalla Costa I , Gavoci A , Iyer A , Roccuzzo M , Otto TA , Oliani E , Bridi S , Strohbuecker S , Santos-Rodriguez G , Valdembri D , Serini G , Abreu-Goodger C , Baudet ML .

The Giovanni Armenise-Harvard Foundation, 618969 Seventh Framework Programme, RBSI144NZ4 Ministero dell'Istruzione, dell'Università e della Ricerca (MIUR), EC | Erasmus+, Università degli Studi di Trento (UNITN), 21315 Associazione Italiana per la Ricerca sul Cancro (AIRC), 20366 Associazione Italiana per la Ricerca sul Cancro (AIRC)

	Figure 1. Molecular beacons are new, specific tools to detect endogenous pre‐miRNAs in cells A. B, C. D. E. F. G. H. I. J. K. M. N. O.
	Figure 2. Endogenous and exogenous pre‐miRNAs are actively trafficked along axon microtubules Schematic representation of the experimental paradigm. Concentrations used are as follows: 5 μM MB; 200–250 ng/μl cy3‐pre‐miR‐181a‐1. MB, molecular beacon.Representative image of a single distal RGC axon from MB‐electroporated retina. Growth cone wrist and central domain are indicated with white arrow and star, respectively. Dashed white line delineates the axon. MB, molecular beacon. Scale bars: 5 μm.Illustrative kymograph. Scale bars: 5 μm.Frequency distribution (in percentage) of MB (endo) and cy3‐pre‐miR‐181a‐1 (exo) puncta along the RGC axon shaft. Each data point corresponds to one independent experiment. Total number of puncta and axons analyzed is as follows: 353 puncta and 20 axons (endo); 484 puncta and 29 axons (exo). n = 3 (endo) and n = 4 (exo) independent experiments. Values are mean ± SEM. MB, molecular beacon; ns, not significant.Average velocity of MB (endo) and cy3‐pre‐miR‐181a‐1 (exo) puncta. Each data point corresponds to one punctum. Total number of puncta and axons analyzed is as follows: 353 puncta and 20 axons (endo); 484 puncta and 29 axons (exo). n = 3 (endo) and n = 4 (exo) independent experiments. Values are median with interquartile range. MB, molecular beacon; ns, not significant; antero, anterograde movement; retro, retrograde movement.MSD data for MB (endo) and cy3‐pre‐miR‐181a‐1 (exo) tracked particles were fitted with an anomalous diffusion model and α thus calculated (red). Total number of particles and axons analyzed is as follows: 67 particles and 20 axons (endo); 82 particles and 29 axons (exo). n = 3 (endo) and n = 4 (exo) independent experiment. Values are mean ± SEM. MB, molecular beacon.MSD alpha‐coefficient distribution for each single MB (endo) and cy3‐pre‐miR‐181a‐1 (exo) tracked particle. Each data point corresponds to one particle. Total number of particles and axons analyzed is as followed: 67 particles and 20 axons (endo); 82 particles and 29 axons (exo). n = 3 (endo) and n = 4 (exo) independent experiments. Values are median with interquartile range. MB, molecular beacon; ns, not significant.Relative frequency distribution (percentage) of MB (endo) and cy3‐pre‐miR‐181a‐1 (exo) tracked particles. Each data point corresponds to one independent experiment. Total number of particles and axons analyzed is as follows: 67 particles and 20 axons (endo); 82 particles and 29 axons (exo). n = 3 (endo) and n = 4 (exo) independent experiments. Values are mean ± SEM. MB, molecular beacon; ns, not significant.Schematic representation of the experimental paradigm. Five micromolar MB was electroporated. MB, molecular beacon.Representative kymographs before nocodazole (top panel; −Noco) and 30 min after 2.4 μM Noco bath application (bottom panel; +Noco). Stationary puncta in both panels are indicated with black arrows. Scale bars: 5 μm.Frequency distribution (in percentage) of MB punctum speed. Each data point corresponds to one independent experiment. Total number of puncta and axons analyzed is as follows: 358 puncta and 25 axons (−Noco); 503 puncta and 34 axons (+Noco). n = 3 independent experiments. Values are mean ± SEM. MB, molecular beacon; ns, not significant; Noco, nocodazole.Frequency distribution of MB punctum speed. Each data point corresponds to one punctum. Total number of puncta and axons analyzed is as follows: 358 puncta and 25 axons (−Noco); 503 puncta and 34 axons (+Noco). n = 3 independent experiments. Values are median with interquartile range. MB, molecular beacon; ns, not significant; Noco, nocodazole.Data information: **P < 0.01, ****P < 0.0001. Two‐way ANOVA followed by Sidak's multiple comparison post hoc test (D, K). Two‐way ANOVA followed by Tukey's multiple comparison post hoc test (E, H). Data were not normally distributed (Shapiro–Wilk test). Two‐tailed Mann–Whitney test (G, L).
	Figure EV1. Pre‐miRNAs are actively trafficked along microtubules Representative tracked particles. The dashed white lines delineate the axon. MB, molecular beacon. Scale bars: 10 μm.Representative tracked particles. The x‐y trajectory for each motion type is represented within the axon. Note the difference in trajectory length according to the particle type. The dashed black lines delineate the axon.High spatial resolution of x, y displacement for each motion type and corresponding MSD plot. Most trajectories analyzed displayed a perfect or near‐perfect fitting reflecting a single‐mode behavior. Note the striking difference in trajectories according to particle type. Only a small portion of the actively moving particle trajectory is shown in the yellow inset. Scale bars: 1 μmx1μm.Mean cy3‐pre‐miR‐181a‐1 puncta speed before and 30 min after vincristine bath application. Concentration used is as follows: 0.1 μM vincristine. Each data point corresponds to one punctum. Total number of puncta and axons analyzed is as follows: 397 puncta and 15 axons (−vincristine); 257 puncta and 15 axons (+vincristine). n = 3 independent experiments. Values are median with interquartile range.Frequency distribution (in percentage) of cy3‐pre‐miR‐181a‐1 puncta per speed categories before and 30 min after vincristine bath application. Concentration used is as follows: 0.1 μM vincristine. Each data point corresponds to one independent experiment. Total number of puncta and axons analyzed is as follows: 397 puncta and 15 axons (−vincristine); 257 puncta and 15 axons (+vincristine). n = 3 independent experiments. Values are mean ± SEM. ns, not significant.Data information: ****P < 0.0001. Data were not normally distributed (Shapiro–Wilk test) (D, E). Two‐tailed Mann–Whitney test (D). Two‐way ANOVA followed by Sidak's multiple comparison test (E).
	Figure 3. Pre‐miRNAs are trafficked along microtubules associated with vesicles A. B. C. D. E. F. G. H. I. J. K, L.
	Figure 4. pre‐miR‐181a‐1 is trafficked docked to late endosomes/lysosomes Schematic representation of the experimental paradigm. Plasmid concentrations used are as follows: 0.5 μg/μl pCS2‐CD63‐eGFP, pCS2‐CD63‐mRFP, pCS2‐Rab7a‐mRFP, or pCS2‐Lamp1‐eGFP; 0.4 μg/μl pCS2‐Rab7a‐eGFP or pCS2‐Rab5a‐mRFP; 0.3 μg/μl pCS2‐Rab5a‐eGFP; 50 nM LysoTracker; 200 ng/μl cy3‐pre‐miR‐181a‐1 or cy5‐pre‐miR‐181a‐1.Overview of the markers used. Figure adapted from Ref. (Yap et al, 2018). EE, early endosome; LE, late endosome; Ly, lysosome.Representative images of co‐electroporated axons. Dashed white lines delineate axons. White arrows indicate colocalized puncta. Colored arrows represent non‐colocalized signal as follows: magenta for CD63 and yellow for Lamp1 or Rab5a. CD63, CD63‐eGFP or CD63‐mRFP; Lamp1, Lamp1‐eGFP; Rab5a, Rab5a‐eGFP or Rab5a‐mRFP. Scale bars: 5 μm.Frequency (in percentage) of CD63 colocalization with specific organelle markers. Each data point corresponds to one axon. Total number of puncta, axons, and independent experiments analyzed is as follows: 540 puncta, 23 axons, and n = 4 (CD63/Rab7a); 416 puncta, 18 axons, and n = 3 (CD63/LysoTracker); 584 puncta, 17 axons, and n = 2 (CD63/Lamp1); 649 puncta, 19 axons, and n = 3 (CD63/Rab5a). Values are mean ± SEM. CD63, CD63‐eGFP or CD63‐mRFP; Lamp1, Lamp1‐eGFP; Rab5a, Rab5a‐eGFP or Rab5a‐mRFP; Rab7a, Rab7a‐eGFP or Rab7a‐mRFP.Representative images of co‐electroporated axons. Dashed white lines delineate axons. White arrows indicate colocalized puncta. Colored arrows represent non‐colocalized signal as follows: cyan for pre‐miR‐181a‐1 and yellow for Lamp1 or Rab5a. Lamp1, Lamp1‐eGFP; Rab5a, Rab5a‐eGFP or Rab5a‐mRFP; pre‐miR‐181a‐1, cy3‐pre‐miR‐181a‐1 or cy5‐pre‐miR‐181a‐1. Scale bars: 5 μm.Frequency (in percentage) of pre‐miR‐181a‐1 colocalization with specific organelle markers. Each data point corresponds to one axon. Total number of puncta, axons, and independent experiments analyzed is as follows: 825 puncta, 41 axons, and n = 8 (pre‐miR‐181a‐1/CD63); 732 puncta, 33 axons, and n = 7 (pre‐miR‐181a‐1/Rab7a); 681 puncta, 29 axons, and n = 5 (pre‐miR‐181a‐1/LysoTracker); 501 puncta, 17 axons, and n = 2 (pre‐miR‐181a‐1/Lamp1); 791 puncta, 25 axons, and n = 3 (pre‐miR‐181a‐1/Rab5a). Values are median with interquartile range. CD63, CD63‐eGFP or CD63‐mRFP; Rab7a, Rab7a‐eGFP or Rab7a‐mRFP; Lamp1, Lamp1‐eGFP; Rab5a, Rab5a‐eGFP or Rab5a‐mRFP; pre‐miR‐181a‐1, cy3‐pre‐miR‐181a‐1 or cy5‐pre‐miR‐181a‐1.Representative images of co‐electroporated axons. Dashed white lines delineate axons. White arrows indicate colocalized puncta. Colored arrows represent non‐colocalized signal as follows: magenta for CD63, cyan for pre‐miR‐181a‐1, yellow for Rab7a, and blue for LysoTracker. CD63, CD63‐eGFP or CD63‐mRFP; Rab7a, Rab7a‐eGFP or Rab7a‐mRFP; pre‐miR‐181a‐1, cy3‐pre‐miR‐181a‐1 or cy5‐pre‐miR‐181a‐1. Scale bar: 5 μm.Frequency (in percentage) of pre‐miR‐181a‐1 colocalization with vesicles double‐positive for organelle markers. Each data point corresponds to one axon. Total number of puncta, axons, and independent experiments analyzed is as follows: 745 puncta, 23 axons, and n = 5 (CD63/pre‐miR‐181a‐1/Rab7a); and 577 puncta, 18 axons, and n = 3 (CD63/pre‐miR‐181a‐1/LysoTracker). Values are median with interquartile range. ns, not significant; CD63, CD63‐eGFP or CD63‐mRFP; Rab7a, Rab7a‐eGFP or Rab7a‐mRFP; pre‐miR‐181a‐1, cy3‐pre‐miR‐181a‐1 or cy5‐pre‐miR‐181a‐1.Representative 3D‐STED super‐resolution image. Total number of puncta, axons, and growth cones analyzed is as follows : 99 puncta, 16 axons, and 10 growth cones (MB); 291 puncta, 36 axons, and 15 growth cones (cy3‐pre‐miR‐181a‐1). n = 2 (MB) and n = 3 (cy3‐pre‐miR‐181a‐1) independent experiments. CD63, CD63‐eGFP; pre‐miR‐181a‐1, cy3‐pre‐miR‐181a‐1; MB; molecular beacon. Scale bars: 200 nm.Data information: ****P < 0.0001. Values were normally distributed (Shapiro–Wilk test). One‐way ANOVA with Tukey's multiple comparison post hoc test (D). Values were not normally distributed (Shapiro–Wilk test) (F, H). Kruskal–Wallis test with Dunn's multiple comparison post hoc test (F). Two‐tailed Mann–Whitney test (H).
	Figure 5. Dicer and Ago2 are present within axons Schematic representation of the experimental protocol.Representative Xenopus growth cones stained with anti‐Dicer and anti‐Ago2. White dashed lines delineate growth cones. Scale bars: 5 μm.Representative E13.5 mice brain cross‐section (dashed red line in the schematic) comprising the optic nerve (ON) stained with anti‐neurofilament and anti‐HA antibodies to detect RGC axons and (FLAG‐HA2)‐Dicer, respectively. Note the absence of HA signal in wild‐type (WT) mice. The white dashed line delineates the ON. Zoom of the triple‐stained ON (right panel): Dicer signal is detected inside ON cells surrounding axon bundles but not in axons per se (arrowheads). n = 3 independent experiments. WT, wild type; HA, (FLAG‐HA2)‐Dicer; E13.5, embryonic day 13.5; ONH, optic nerve head; ON, optic nerve. Scale bars: 30 μm.Representative P0 superior colliculus stratum griseum superficiale (SGS; sagittal sectioning of P0 brains along the dashed red line in the schematic, maximal projection of 5 μm depth). Note the presence of Dicer within the SGS marked with neurofilament. n = 3 independent experiments. WT, wild type; P0, postnatal day 0. Scale bars: 30 μm.
	Figure EV2. Dicer is present in RGC axonal compartment Schematic of FLAG‐HA2‐Dicer. Red arrows indicate primers used for the genotyping spanning the FLAG‐HA2 region. WT, wild type; HA, (FLAG‐HA2)‐Dicer.Genotyping PCR. WT, wild type; HA, (FLAG‐HA2)‐Dicer; P0, postnatal day 0; E13.5, embryonic day 13.5.Representative E13.5 retina stained for anti‐HA antibody. Dashed light blue box indicates the region zoomed. WT, wild type; E13.5, embryonic day 13.5. Scale bars: 50 μm.Representative P0 superior colliculus stained with anti‐neurofilament and anti‐HA antibodies to detect RGC axons in the stratum griseum superficiale of the superior colliculus and (FLAG‐HA2)‐Dicer, respectively. Dashed white box indicates the region zoomed. Zoom of the triple‐stained P0 superior colliculus in a nucleus‐free region. WT, wild type; P0, postnatal day 0. Scale bars: 30 μm. Source data are available online for this figure.
	Figure 6. Pre‐miRNAs are processed locally in response to cues and newly generated miRNAs are important for growth cone steering ex vivo A. B, C. D. E, F.
	Figure EV3. The fast transport of pre‐miR‐181a‐1 is decreased upon Sema3A exposure A. B–D. E. F.
	Figure EV4. Morpholino mix validation A. B, C. D. E–G.
	Figure 7. Mature miRNAs are important for axon targeting in vivo and for a fully functional visual system Schematic representation of the experimental paradigm. Concentrations used are as follows: 0.5 μg/μl pCS2‐mCherry plasmid; 250 μM miR‐181‐MO or control MO cocktail. co‐MO, control morpholino.Representative images of RGC axons within the optic tectum. A subset of aberrantly projecting axons are indicated (red arrows). Note that a few straying axons are always observed within the wild‐type tectum. co‐MO, control morpholino. Scale bars: 20 μm.Quantification of misprojecting axons. Each data point corresponds to one brain. Total number of brains analyzed is as follows: 45 brains (co‐MO) and 52 brains (miR‐181‐MO). n = 4 independent experiments. Values are mean ± SEM. co‐MO, control morpholino.Schematic representation of the experimental paradigm. Concentrations used are as follows: 0.5 μg/μl pCS2‐mCherry or pCS2‐eGFP plasmids; 250 μM miR‐181‐MO or control MO cocktail; 50 μM miR‐181 or control mimics (top). Representative images of RGC axons within the optic tectum. White arrows indicate axons targeted both by MO (green) and by miRNA mimics (red; bottom). co‐MO, control morpholino. Scale bars: 20 μm.Quantification of misprojecting axons. The number reported on the bars is the total number of co‐electroporated axons. Note how miR‐181 mimics rescued aberrant misprojection of morphant axons in vivo. Each data point corresponds to one independent experiment. Total number of axons and brains analyzed is as follows: 96 axons and 4 brains (co‐MO + ctrl mimics); 101 axons and 4 brains (miR‐181‐MO + ctrl mimics), 134 axons and 4 brains (miR‐181‐MO + miR‐181 mimics). n = 4 independent experiments. Values are mean ± SEM. co‐MO, control morpholino; ns, not significant.Representative images of RGC axons within the optic tectum. A subset of aberrantly projecting axons are indicated (red arrows). Note that a few straying axons are always observed within the wild‐type tectum. co‐MO, control morpholino. Scale bars: 20 μm.Quantification of misprojecting axons. Each data point corresponds to one brain. Total number of brains analyzed is as follows: 21 brains (co‐MO) and 31 brains (miR‐181‐MO). n = 3 independent experiments. Values are mean ± SEM. co‐MO, control morpholino.Schematic representation of the experimental paradigm. Concentrations used are as follows: 0.5 μg/μl pCS2‐eGFP plasmid; 250 μM miR‐181‐MO or control MO cocktail. co‐MO, control morpholino.Frequency (in percentage) of the amount of time embryos spent on black background. Each data point corresponds to one embryo. Total number of embryos analyzed is as follows: 43 embryos (co‐MO) and 45 embryos (miR‐181‐MO). n = 4 independent experiments. Values are mean ± SEM. co‐MO, control morpholino.Data Information: *P < 0.05, **P < 0.01, ****P < 0.001. Data were not normally distributed (Shapiro–Wilk test). Two‐tailed Mann–Whitney test (C, G, I). Data were normally distributed (Shapiro–Wilk test). One‐way ANOVA followed by Tukey's multiple comparison post hoc test (E).
	Figure 8. Newly generated miRNAs silence the locally translated transcript TUBB3 A. B–G. H, I.
	Figure EV5. FRAP construct and experimental paradigm Schematic of Venus‐3′UTR constructs used as reporters of axonal translation in FRAP experiments. ACTB, β‐actin; bp, base pair; TUBB3, tubulin beta 3 class III; APP, amyloid precursor protein; THBS1, thrombospondin 1; wt, wild type.Quantification (in percentage) of the axonal fluorescence recovery after photobleaching (FRAP) of pCS2‐Venus‐ACTB‐3′UTR construct ex vivo using whole explants. Concentration used is as follows: 0.7 μg/μl. Total number of axons analyzed is reported in the legend. n = 3 independent experiments. Values are mean ± SEM. ACTB, β‐actin; CHX, cycloheximide.Representative growth cones depicting Venus fluorescence intensity as a heatmap. Dashed white line delineates the growth cones. ACTB, β‐actin; CHX, cycloheximide; wt, wild type. Scale bars: 10 μm.Schematic representations of the experimental paradigm.Schematic representations of the experimental paradigm. Axons in the vicinity of tectal Sema3A expression territories were selected for FRAP analysis.Data information: ****P < 0.0001. Dashed black lines represent least‐square fits to a single‐exponential decay equation. Extra sum‐of‐squares F‐test. Exact P‐value of all FRAP experiments and row statistics are reported in Table EV3(B).
	Figure 9. Endogenous TUBB3 is a key mediator of NGmiRNA‐mediated Sema3A signaling Schematic representation of puromycin‐proximity ligation assay. Concentration used is as follows: 2 ng/μl (puromycin). TUBB3, tubulin beta 3 class III; PLA probes, proximity ligation assay probes.Schematic representation of the experimental paradigm. Representative images of local translation events of TUBB3 in the growth cone. Dashed white line delineates the growth cone. Each white arrow points to a puro‐PLA puncta. TUBB3, tubulin beta 3 class III; Puro, puromycin. Scale bars: 5 μm.Quantification of number of puncta per growth cone. Each data point corresponds to one growth cone. Total number of growth cones analyzed is as follows: 30 (PBS) and 36 (Sema3A). n = 2 independent experiments. Values are median with interquartile range.Schematic representation of the experimental paradigm. Concentrations used are as follows: 2 μM co‐MO; 2 μM MOs‐3p; 200 ng/ml Sema3A. Representative images of local translation events of TUBB3 in the growth cone of transfected axons. Dashed white line delineates the growth cone. White arrows represent number of puro‐PLA puncta per growth cone. co‐MO, control morpholino. Scale bars: 5 μm.Quantification of number of puncta per growth cone. Each data point corresponds to one growth cone. Total number of growth cones analyzed is as follows: 32 (co‐MO + PBS), 45 (co‐MO + Sema3A), 27 (MOs‐3p + Sema3A). n = 2 independent experiments. Values are median with interquartile range. co‐MO, control morpholino; ns, not significant.Schematic representation of the experimental paradigm. Concentrations used are as follows: 4 μM co‐MO; 2 μM MOs‐3p + 2 μM co‐MO; 2 μM MOs‐3p + 2 μM MOs‐TUBB3; 200 ng/ml Sema3A. co‐MO, control morpholino; TUBB3, tubulin beta 3 class III.Percentage of collapsed growth cones in axons transfected with co‐MO, MOs‐3p + co‐MO, and MOs‐3p + MOs‐TUBB3. Each data point corresponds to one independent experiment. Total number of growth cones counted is as follows: 152 (co‐MO), 155 (MOs‐3p + co‐MO), 179 (MOs‐3p + MOs‐TUBB3). n = 3 independent experiments. Values are mean ± SEM. ns, not significant; co‐MO, control morpholino; TUBB3, tubulin beta 3 class III.Working model: Pre‐miR‐181a‐1 is transported along RGC axons tethered to CD63‐positive late endosomes/lysosomes. Under non‐stimulated conditions, TUBB3 undergoes basal translation in the axonal compartment. Upon Sema3A exposure, pre‐miR‐181a‐1 is locally processed and the expression level of the concomitant newly generated miRNAs increases locally within the growth cone. miR‐181a‐5p, the predominant mature miRNA generated from pre‐miR‐181a‐1, targets TUBB3, thereby silencing protein synthesis through LPS inhibition (LPS‐I). ns, not significant; LE/Ly, late endosomes/lysosomes; LPS, local protein synthesis; LPS‐I, LPS inhibition; TUBB3, tubulin beta 3 class III.Data information: *P < 0.05, **P < 0.01. Data were not normally distributed (Shapiro–Wilk test) (C, E). Two‐tailed Mann–Whitney test (C). Kruskal–Wallis test followed by Dunn's multiple comparison post hoc test (E). Data were normally distributed (Shapiro–Wilk test). One‐way ANOVA followed by Tukey's multiple comparison post hoc test (G).

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