Arl13b regulates Sonic Hedgehog signaling from outside primary cilia
Preprint posted on 23 July 2019 https://www.biorxiv.org/content/10.1101/711671v1
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
Categories: cell biology, developmental biology, evolutionary biology
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).
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
- 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?
- 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?
- Are ARL13B and INPP5E trafficked together (as a complex) into the cilium or does ARL13B subsequently mediate the trafficking of INPP5E?
- 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
Posted on: 15 August 2019 , updated on: 29 October 2021
doi: https://doi.org/10.1242/prelights.13242
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