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Arl13b regulates Sonic Hedgehog signaling from outside primary cilia

Eduardo D. Gigante, Megan R. Taylor, Anna A. Ivanova, Richard A. Kahn, Tamara Caspary

Posted on: 15 August 2019 , updated on: 29 October 2021

Preprint posted on 23 July 2019

Article now published in eLife at http://dx.doi.org/10.7554/eLife.50434

It’s been tricky to tease apart Hedgehog signalling and primary cilia. Now, this recent preprint finds that although ARL13B is abundant in cilia, it regulates Hedgehog signalling from outside the cilium.

Selected by Alex Eve

Background

The non-motile primary cilium acts as a sensor for chemomechanical signals in vertebrates (Ferreira et al., 2019). One of the most widely known examples of this activity is the role of primary cilia in the transduction of the Sonic hedgehog (Shh) signalling pathway. Here, upon ligand binding, the membrane receptor Patched is degraded (Rohatgi et al., 2007), and the GPCR protein Smoothened translocates from its position at the base of the cilium into the cilium itself (Milenkovic et al., 2015; Weiss et al., 2019). Our current understanding is that the cilium acts as a subcellular compartment where Smoothened is exposed to its cognate ligand (likely a sterol) to transduce the downstream Shh signal (Kong et al., 2019). The Shh transcription factor Gli is also transported to the tip of the cilium upon pathway activation, where, presumably, it is processed into an active form that drives transcription of target genes (Santos and Reiter, 2014).

Mutations in Shh signalling components and ciliary proteins frequently have overlapping phenotypes. Whether Shh signalling in cilia-protein mutants is affected primarily because of disruption to cilia structure or function, or whether ciliary proteins are required for Shh signal transduction are challenging questions to address. Given that cilia and Shh signalling are so closely associated in vertebrates, it is surprising that this relationship is not evolutionary conserved (Huangfu, 2006) . In Drosophila, Hedgehog signalling is present and functional, although (almost) all Drosophila cells lack primary cilia (Larkins et al., 2011; Kuzhandaivel et al., 2014). How, why and when such a fundamental aspect of the signalling cascade diverged during the evolution remains an interesting, but unexplained, phenomenon.

Key findings

In this preprint, Gigante and colleagues build upon previous studies on the ARF family GTPase, ARL13B (Mariani et al., 2016) . ARL13B has diverse functions within the cell, with reported roles in endocytic trafficking, regulation of the phospholipid composition of the ciliary membrane, and intraflagellar transport for the construction and maintenance of cilia (Gigante et al., 2019). Mutations in Arl13b are associated with Joubert’s syndrome, characterised by brain development disorders that are probably caused by defects in the structure and function of cilia (Cantagrel et al., 2008). Supporting this theory, deletion of Arl13b in animal models reduces cilia length and impairs Shh signalling (Caspary et al., 2007; Larkins et al., 2011).

1. Ciliary localisation of ARL13B is required for normal cilium length
The authors use CRISPR/Cas9 gene editing in mice to make a point mutation in Arl13b within a known cilia localisation sequence: ARL13BV358A (Mariani et al., 2016). Indeed, immunostaining for ARL13B shows that the protein is excluded from the cilia. By quantifying cilia in mouse embryonic fibroblasts (MEFs), the authors find that the number of ciliated cells and the length of the cilia are decreased in Arl13b-null and Arl13bV358A backgrounds. These data support the known role of ARL13B in cilia development and indicate that this function is dependent on an activity of ARL13B within the cilia.

2. Sonic hedgehog signalling does not require ciliary localisation of ARL13B
Somewhat surprisingly, despite the changes to cilia length, Shh signalling is unaffected and Arl13bV358A embryos develop normally, shown by the expression of Nkx2.2, HB9 and Olig2 in the neural tube. Indeed, Shh components, such as Smoothend, Gli2/3, SuFu and Patched1, localise to the primary cilium of Arl13bV358A MEFs in response to Shh-conditioned media. In Arl13b-null mutants, however, Shh signalling is abolished and components are mis-localised. These data suggest that ARL13B regulates Shh signal transduction from the outside of cilia, possibly by trafficking Smoothened into the cilium. Importantly, this function is independent of ARL13B’s role in ciliogenesis (regulating cilia length).

3. ARL13B regulates the localisation of inositol polyphosphate-5-phosphatase E (Inpp5e) in the cilium
Although Shh signalling components traffic normally in the cilium of Arl13bV358A cells, the authors reveal that INPP5E, which is also implicated in Joubert’s syndrome (Bielas et al., 2009) and in Shh signalling regulation (Dyson et al., 2016), is absent from the cilium. These data indicate that ARL13B is required for INPP5E localisation to the cilia, although INPP5E activity is not required specifically in the cilium for Shh signalling. In a second preprint from the Caspary group, the role of INPP5E in Shh signal transduction is investigated further (Constable et al., 2016).

Figure 1. Model comparing complete loss of ARL13B function to ciliary loss of ARL13B function. Composition of primary cilia with (left-side, +Shh) and without (right-side) Sonic hedgehog signalling in wild type (A), Arl13b-null (Arl13b-hnn), (B) and Arl13b-V358A (C) cells. Taken from Figure 7 of Gigante et al. preprint[11].

 

Why I chose this preprint

The evolutionary relationship between Hedgehog signalling and cilia is a fundamental and interesting problem. In this preprint, the authors successfully dissect one of the many functions of ARL13B and uncouple the functions of ARL13B in Shh signalling and in ciliogenesis. It’s surprising that ARL13B regulates Shh signalling from outside the cilia, which challenges our preconceptions about the protein’s function. In addition, this study proposes a model in which the primary cilium has been co-opted by the Shh signalling pathway during the evolution of vertebrates, coinciding with the duplication of ARL13.

Open questions

  1. It is interesting that Shh signalling can function in cilia of reduced length, are there any other differences to the composition and compartmentalisation of cilia in Arl13bV358A cells?
  2. In adult Drosophila, olfactory sensory neurons (OSNs) are ciliated and Smoothened reportedly translocates to the cilium in response to Hedgehog signalling (Kuzhandaivel et al., 2014). How does this fit with the evolutionary model proposed in the manuscript?
  3. Are ARL13B and INPP5E trafficked together (as a complex) into the cilium or does ARL13B subsequently mediate the trafficking of INPP5E?
  4. Do the Arl13bV358A mice display any other similar phenotypes to those associated with Joubert’s syndrome or ciliopathies?

References

Bielas, S. L., Silhavy, J. L., Brancati, F., Kisseleva, M. V., Al-Gazali, L., Sztriha, L., … Gleeson, J. G. (2009). Mutations in INPP5E, encoding inositol polyphosphate-5-phosphatase E, link phosphatidyl inositol signaling to the ciliopathies. Nature Genetics, 41(9), 1032–1036. https://doi.org/10.1038/ng.423

Cantagrel, V., Silhavy, J. L., Bielas, S. L., Swistun, D., Marsh, S. E., Bertrand, J. Y., … Gleeson, J. G. (2008). Mutations in the Cilia Gene ARL13B Lead to the Classical Form of Joubert Syndrome. The American Journal of Human Genetics, 83(2), 170–179. https://doi.org/10.1016/j.ajhg.2008.06.023

Caspary, T., Larkins, C. E., & Anderson, K. V. (2007). The Graded Response to Sonic Hedgehog Depends on Cilia Architecture. Developmental Cell, 12(5), 767–778. https://doi.org/10.1016/j.devcel.2007.03.004

Constable, S., Long, A. B., Floyd, K. A., Schurmans, S., & Caspary, T. (2019). Ciliary phosphatidylinositol phosphatase Inpp5e plays positive and negative regulatory roles in Shh signaling. Cold Spring Harbor Laboratory. https://doi.org/10.1101/721399

Dyson, J. M., Conduit, S. E., Feeney, S. J., Hakim, S., DiTommaso, T., Fulcher, A. J., … Mitchell, C. A. (2016). INPP5E regulates phosphoinositide-dependent cilia transition zone function. The Journal of Cell Biology, 216(1), 247–263. https://doi.org/10.1083/jcb.201511055

Ferreira, R., Fukui, H., Chow, R., Vilfan, A., & Vermot, J. (2019). The cilium as a force sensor−myth versus reality. Journal of Cell Science, 132(14), jcs213496. https://doi.org/10.1242/jcs.213496

Gigante, E. D., Taylor, M. R., Ivanova, A. A., Kahn, R. A., & Caspary, T. (2019). Arl13b regulates Sonic Hedgehog signaling from outside primary cilia. Cold Spring Harbor Laboratory. https://doi.org/10.1101/711671

Huangfu, D. (2006). Signaling from Smo to Ci/Gli: conservation and divergence of Hedgehog pathways from Drosophila to vertebrates. Development, 133(1), 3–14. https://doi.org/10.1242/dev.02169

Kong, J. H., Siebold, C., & Rohatgi, R. (2019). Biochemical mechanisms of vertebrate hedgehog signaling. Development, 146(10), dev166892. https://doi.org/10.1242/dev.166892

Kuzhandaivel, A., Schultz, S. W., Alkhori, L., & Alenius, M. (2014). Cilia-Mediated Hedgehog Signaling in Drosophila. Cell Reports, 7(3), 672–680. https://doi.org/10.1016/j.celrep.2014.03.052

Rohatgi, R., Milenkovic, L., & Scott, M. P. (2007). Patched1 Regulates Hedgehog Signaling at the Primary Cilium. Science, 317(5836), 372–376. https://doi.org/10.1126/science.1139740

Larkins, C. E., Aviles, G. D. G., East, M. P., Kahn, R. A., & Caspary, T. (2011). Arl13b regulates ciliogenesis and the dynamic localization of Shh signaling proteins. Molecular Biology of the Cell, 22(23), 4694–4703. https://doi.org/10.1091/mbc.e10-12-0994

Mariani, L. E., Bijlsma, M. F., Ivanova, A. A., Suciu, S. K., Kahn, R. A., & Caspary, T. (2016). Arl13b regulates Shh signaling from both inside and outside the cilium. Molecular Biology of the Cell, 27(23), 3780–3790. https://doi.org/10.1091/mbc.e16-03-0189

Milenkovic, L., Weiss, L. E., Yoon, J., Roth, T. L., Su, Y. S., Sahl, S. J., … Moerner, W. E. (2015). Single-molecule imaging of Hedgehog pathway protein Smoothened in primary cilia reveals binding events regulated by Patched1. Proceedings of the National Academy of Sciences, 112(27), 8320–8325. https://doi.org/10.1073/pnas.1510094112

Santos, N., & Reiter, J. F. (2014). A central region of Gli2 regulates its localization to the primary cilium and transcriptional activity. Journal of Cell Science, 127(7), 1500–1510. https://doi.org/10.1242/jcs.139253

Weiss, L. E., Milenkovic, L., Yoon, J., Stearns, T., & Moerner, W. E. (2019). Motional dynamics of single Patched1 molecules in cilia are controlled by Hedgehog and cholesterol. Proceedings of the National Academy of Sciences, 116(12), 5550–5557. https://doi.org/10.1073/pnas.1816747116

Tags: arl13b, cilia, ciliogenesis, ciliopathies, evolution, hedgehog

doi: https://doi.org/10.1242/prelights.13242

Read preprint (1 votes)

Author's response

Tamara Caspary shared

It is interesting that Shh signalling can function in cilia of reduced length, are there any other differences to the composition and compartmentalisation of cilia in Arl13bV358A cells?

  • We have yet to examine the Arl13bV358A cilia in more depth. Our previous analysis of the null allele, Arl13bhnn, showed an architectural defect in the B tubules of the microtubule doublets and altered glutamylated and acetylated tubulin levels within cilia so it those would be the phenotypes to prioritize examining.

In adult Drosophila, olfactory sensory neurons (OSNs) are ciliated and Smoothened reportedly translocates to the cilium in response to Hedgehog signalling8. How does this fit with the evolutionary model proposed in the manuscript?

  • Our model is primarily based on the observation that the duplication of ARL13 into ARL13A and ARL13B occurred in the urochordates at about the same time that Hh signalling became dependent on cilia so is entirely speculative at this point. The requirement of intraflagellar transport to enrich SMO in Drosophila OSN cilia is provocative yet several labs have used multiple techniques and concluded that Hh signal transduction does not use cilia in Drosophila. Additionally, we previously published a hypomorphic allele of Smo, cabbie, that does pretty well at transducing Shh signalling yet doesn’t efficiently enrich in cilia so it is not entirely clear how to interpret SMO ciliary enrichment in mammals. To our knowledge, Arl13 mutants in flies have not yet been examined for any phenotypes, including Hh-related phenotypes.

Are ARL13B and INPP5E trafficked together (as a complex) into the cilium or does ARL13B subsequently mediate the trafficking of INPP5E?

  • Previous work by Humbert et al. (PNAS, 2012) showed ARL13B, Inpp5e and PDE6D in a common complex and ARL13B being required for cilia enrichment of INPP5E. As ARL13B is also highly enriched in cilia the assumption has been that the complex is trafficked to cilia yet our data suggest that may not be true. While Joubert-causing mutations disrupt the ARL13B-INPP5E protein interaction, we have not tested whether the ARL13BV358A mutation (which is not a known Joubert-causing allele) retains its interaction with INPP5E; we know that ARL13BV358A retains all known biochemical activities.

Do the Arl13bV358A mice display any other similar phenotypes to those associated with Joubert’s syndrome or ciliopathies?

  • We’re certainly curious if these mice display common phenotypes consistent with mouse models of Joubert and other ciliopathies- so we plan to look.

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Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20

 



List by Maiko Kitaoka et al.

ECFG15 – Fungal biology

Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome

 



List by Hiral Shah

COVID-19 / SARS-CoV-2 preprints

List of important preprints dealing with the ongoing coronavirus outbreak. See http://covidpreprints.com for additional resources and timeline, and https://connect.biorxiv.org/relate/content/181 for full list of bioRxiv and medRxiv preprints on this topic

 



List by Dey Lab, Zhang-He Goh

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SDB 78th Annual Meeting 2019

A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.

 



List by Alex Eve

Pattern formation during development

The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.

 



List by Alexa Sadier
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