Browse > Article
http://dx.doi.org/10.14348/molcells.2020.0205

Sub-Ciliary Segregation of Two Drosophila Transient Receptor Potential Channels Begins at the Initial Stage of Their Pre-Ciliary Trafficking  

Kwon, Youngtae (Department of Life Sciences, University of Seoul)
Lee, Jeongmi (Department of Life Sciences, University of Seoul)
Chung, Yun Doo (Department of Life Sciences, University of Seoul)
Publication Information
Molecules and Cells / v.43, no.12, 2020 , pp. 1002-1010 More about this Journal
Abstract
Cilia are important eukaryotic cellular compartments required for diverse biological functions. Recent studies have revealed that protein targeting into the proper ciliary subcompartments is essential for ciliary function. In Drosophila chordotonal cilium, where mechano-electric transduction occurs, two transient receptor potential (TRP) superfamily ion channels, TRPV and TRPN, are restricted to the proximal and distal subcompartments, respectively. To understand the mechanisms underlying the sub-ciliary segregation of the two TRPs, we analyzed their localization under various conditions. In developing chordotonal cilia, TRPN was directly targeted to the ciliary tip from the beginning of its appearance and was retained in the distal subcompartment throughout development, whereas the ciliary localization of TRPV was considerably delayed. Lack of intraflagella transport-related proteins affected TRPV from the initial stage of its pre-ciliary trafficking, whereas it affected TRPN from the ciliary entry stage. The ectopic expression of the two TRP channels in both ciliated and non-ciliated cells revealed their intrinsic properties related to their localization. Taken together, our results suggest that sub-ciliary segregation of the two TRP channels relies on their distinct intrinsic properties, and begins at the initial stage of their pre-ciliary trafficking.
Keywords
cilia; ciliary sub-compartment; Drosophila; intraflagella transport; transient receptor potential channel;
Citations & Related Records
Times Cited By KSCI : 3  (Citation Analysis)
연도 인용수 순위
1 Eberl, D.F., Hardy, R.W., and Kernan, M.J. (2000). Genetically similar transduction mechanisms for touch and hearing in Drosophila. J. Neurosci. 20, 5981-5988.   DOI
2 Follit, J.A., Tuft, R.A., Fogarty, K.E., and Pazour, G.J. (2006). The intraflagellar transport protein IFT20 is associated with the Golgi complex and is required for cilia assembly. Mol. Biol. Cell 17, 3781-3792.   DOI
3 Lee, J. and Chung, Y.D. (2015). Ciliary subcompartments: how are they established and what are their functions? BMB Rep. 48, 380-387.   DOI
4 Lee, J., Moon, S., Cha, Y., and Chung, Y.D. (2010). Drosophila TRPN (=NOMPC) channel localizes to the distal end of mechanosensory cilia. PLoS One 5, e11012.   DOI
5 Lee, N., Park, J., Bae, Y.C., Lee, J.H., Kim, C.H., and Moon, S.J. (2018). Timelapse live-cell imaging reveals dual function of Oseg4, Drosophila WDR35, in ciliary protein trafficking. Mol. Cells 41, 676-683.   DOI
6 Venken, K.J., He, Y., Hoskins, R.A., and Bellen, H.J. (2006). P[acman]: a BAC transgenic platform for targeted insertion of large DNA fragments in D. melanogaster. Science 314, 1747-1751.   DOI
7 Sharma, Y., Cheung, U., Larsen, E.W., and Eberl, D.F. (2002). pPTGAL, a convenient Gal4 P-element vector for testing expression of enhancer fragments in Drosophila. Genesis 34, 115-118.   DOI
8 Sung, C.H. and Leroux, M.R. (2013). The roles of evolutionarily conserved functional modules in cilia-related trafficking. Nat. Cell Biol. 15, 1387-1397.   DOI
9 Taschner, M. and Lorentzen, E. (2016). The intraflagellar transport machinery. Cold Spring Harb. Perspect. Biol. 8, a028092.   DOI
10 Chung, Y.D., Zhu, J., Han, Y., and Kernan, M.J. (2001). nompA encodes a PNS-specific, ZP domain protein required to connect mechanosensory dendrites to sensory structures. Neuron 29, 415-428.   DOI
11 Jin, H., White, S.R., Shida, T., Schulz, S., Aguiar, M., Gygi, S.P., Bazan, J.F., and Nachury, M.V. (2010). The conserved Bardet-Biedl syndrome proteins assemble a coat that traffics membrane proteins to cilia. Cell 141, 1208-1219.   DOI
12 Gong, Z., Son, W., Chung, Y.D., Kim, J., Shin, D.W., McClung, C.A., Lee, Y., Lee, H., Chang, D.J., Kaang, B.K., et al. (2004). Two interdependent TRPV channel subunits, Inactive and Nanchung, mediate hearing in Drosophila. J. Neurosci. 24, 9059-9066.   DOI
13 Gopfert, M.C., Albert, J.T., Nadrowski, B., and Kamikouchi, A. (2006). Specification of auditory sensitivity by Drosophila TRP channels. Nat. Neurosci. 9, 999-1000.   DOI
14 Hartenstein, V. (1988). Development of Drosophila larval sensory organs: spatiotemporal pattern of sensory neurones, peripheral axonal pathways and sensilla differentiation. Development 102, 869-886.   DOI
15 Kim, J., Chung, Y.D., Park, D.Y., Choi, S., Shin, D.W., Soh, H., Lee, H.W., Son, W., Yim, J., Park, C.S., et al. (2003). A TRPV family ion channel required for hearing in Drosophila. Nature 424, 81-84.   DOI
16 Lee, E., Sivan-Loukianova, E., Eberl, D.F., and Kernan, M.J. (2008). An IFT-A protein is required to delimit functionally distinct zones in mechanosensory cilia. Curr. Biol. 18, 1899-1906.   DOI
17 Park, J., Lee, J., Shim, J., Han, W., Lee, J., Bae, Y.C., Chung, Y.D., Kim, C.H., and Moon, S.J. (2013). dTULP, the Drosophila melanogaster homolog of tubby, regulates transient receptor potential channel localization in cilia. PLoS Genet. 9, e1003814.   DOI
18 Lehnert, B.P., Baker, A.E., Gaudry, Q., Chiang, A.S., and Wilson, R.I. (2013). Distinct roles of TRP channels in auditory transduction and amplification in Drosophila. Neuron 77, 115-128.   DOI
19 Mazelova, J., Astuto-Gribble, L., Inoue, H., Tam, B.M., Schonteich, E., Prekeris, R., Moritz, O.L., Randazzo, P.A., and Deretic, D. (2009). Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4. EMBO J. 28, 183-192.   DOI
20 Morthorst, S.K., Christensen, S.T., and Pedersen, L.B. (2018). Regulation of ciliary membrane protein trafficking and signalling by kinesin motor proteins. FEBS J. 285, 4535-4564.   DOI
21 Patel, N.H. (1994). Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. In Drosophila melanogaster: Practical Uses in Cell and Molecular Biology, L.S.B. Goldstein and E.A. Fyrberg, eds. (London, UK: Academic Press), pp. 445-487.
22 Yan, Z., Zhang, W., He, Y., Gorczyca, D., Xiang, Y., Cheng, L.E., Meltzer, S., Jan, L.Y., and Jan, Y.N. (2012). Drosophila NOMPC is a mechanotransduction channel subunit for gentle-touch sensation. Nature 493, 221-225.   DOI
23 Walker, R.G., Willingham, A.T., and Zuker, C.S. (2000). A Drosophila mechanosensory transduction channel. Science 287, 2229-2234.   DOI
24 Waters, A.M. and Beales, P.L. (2011). Ciliopathies: an expanding disease spectrum. Pediatr. Nephrol. 26, 1039-1056.   DOI
25 Wright, K.J., Baye, L.M., Olivier-Mason, A., Mukhopadhyay, S., Sang, L., Kwong, M., Wang, W., Pretorius, P.R., Sheffield, V.C., Sengupta, P., et al. (2011). An ARL3-UNC119-RP2 GTPase cycle targets myristoylated NPHP3 to the primary cilium. Genes Dev. 25, 2347-2360.   DOI