Dopamine receptors reveal an essential role of IFT-B, KIF17, and Rab23 in delivering specific receptors to primary cilia

eLife

Volumn 4, Issue JULY2015, 2015, Pages

  Leaf, Alison ^a,b   Von Zastrow, Mark ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CILIARY KINESIN KIF17; DELTA OPIATE RECEPTOR; DOPAMINE 1 RECEPTOR; INTRAFLAGELLAR TRANSPORT COMPLEX B PROTEIN; PEPTIDES AND PROTEINS; RAB23 PROTEIN; SOMATOSTATIN RECEPTOR 3; UNCLASSIFIED DRUG; CARRIER PROTEIN; DOPAMINE RECEPTOR; KIF17 PROTEIN, MOUSE; KINESIN; RAB PROTEIN; RAB23 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CILIATED EPITHELIUM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EPIFLUORESCENCE MICROSCOPY; FLOW CYTOMETRY; IMAGE ANALYSIS; IMMUNOREACTIVITY; MOTOR ACTIVITY; MOUSE; NONHUMAN; PHENOTYPE; PHOTOACTIVATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SITE DIRECTED MUTAGENESIS; WESTERN BLOTTING; ANIMAL; EUKARYOTIC FLAGELLUM; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

ANIMALS; CARRIER PROTEINS; CILIA; KINESIN; MICE; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RECEPTORS, DOPAMINE;

EID: 84940541319     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.06996     Document Type: Article

References (52)

1. Berbari NF, Johnson AD, Lewis JS, Askwith CC, Mykytyn K. 2008a. Identification of ciliary localization sequences within the third intracellular loop of G protein-coupled receptors. Molecular Biology of the Cell 19:1540-1547. doi: 10.1091/mbc.E07-09-0942.
2. Berbari NF, Lewis JS, Bishop GA, Askwith CC, Mykytyn K. 2008b. Bardet-biedl syndrome proteins are required for the localization of G protein-coupled receptors to primary cilia. Proceedings of the National Academy of Sciences of USA 105:1-5. doi: 10.1073/pnas.0711027105.
3. Boehlke C, Bashkurov M, Buescher A, Krick T, John AK, Nitschke R, Walz G, Kuehn EW. 2010. Differential role of Rab proteins in ciliary trafficking: Rab23 regulates smoothened levels. Journal of Cell Science 123:1460-1467. doi: 10.1242/jcs.058883.
4. Chih B, Liu P, Chinn Y, Chalouni C, Komuves LG, Hass PE, Sandoval W, Peterson AS. 2011. A ciliopathy complex at the transition zone protects the cilia as a privileged membrane domain. Nature Cell Biology 14:61-72. doi: 10. 1038/ncb2410.
5. Corbit KC, Aanstad P, Singla V, Norman AR, Stainier DYR, Reiter JF. 2005. Vertebrate smoothened functions at the primary cilium. Nature 437:1018-1021. doi: 10.1038/nature04117.
6. Crouse JA, Lopes VS, Sanagustin JT, Keady BT, Williams DS, Pazour GJ. 2014. Distinct functions for IFT140 and IFT20 in opsin transport. Cytoskeleton 71:302-310. doi: 10.1002/cm.21173.
7. Deretic D, Papermaster DS. 1991. Polarized sorting of rhodopsin on post-Golgi membranes in frog retinal photoreceptor cells. The Journal of Cell Biology 113:1281-1293. doi: 10.1083/jcb.113.6.1281.
8. Deretic D, Schmerl S, Hargrave PA, Arendt A, McDowell JH. 1998. Regulation of sorting and post-Golgi trafficking of rhodopsin by its C-terminal sequence QVS(A)PA. Proceedings of the National Academy of Sciences of USA 95: 10620-10625. doi: 10.1073/pnas.95.18.10620.
9. Deretic D, Williams AH, Ransom N, Morel V, Hargrave PA, Arendt A. 2005. Rhodopsin C terminus, the site of mutations causing retinal disease, regulates trafficking by binding to ADP-ribosylation factor 4 (ARF4). Proceedings of the National Academy of Sciences of USA 102:3301-3306. doi: 10.1073/pnas.0500095102.
10. Domire JS, Green JA, Lee KG, Mykytyn K. 2011. Dopamine receptor 1 localizes to neuronal cilia in a dynamic process that requires the Bardet-Biedl syndrome proteins. Growth 6:2951-2960. doi: 10.1007/s00018-010-0603-4.
11. Eggenschwiler JT, Bulgakov OV, Qin J, Li T, Anderson KV. 2006. Mouse Rab23 regulates hedgehog signaling from smoothened to Gli proteins. Developmental Biology 290:1-12. doi: 10.1016/j.ydbio.2005.09.022.
12. Eggenschwiler JT, Espinoza E, Anderson KV. 2001. Rab23 is an essential negative regulator of the mouse Sonic hedgehog signalling pathway. Nature 412:194-198. doi: 10.1038/35084089.
13. Emmer BT, Maric D, Engman DM. 2010. Molecular mechanisms of protein and lipid targeting to ciliary membranes. Journal of Cell Science 123:529-536. doi: 10.1242/jcs.062968.
14. Follit JA, Xu F, Keady BT, Pazour GJ. 2009. Characterization of mouse IFT complex B. Cell Motility and the Cytoskeleton 66:457-468. doi: 10.1002/cm.20346.
15. Francis SS, Sfakianos J, Lo B, Mellman I. 2011. A hierarchy of signals regulates entry of membrane proteins into the ciliary membrane domain in epithelial cells. Cell 193:219-233. doi: 10.1083/jcb.201009001.
16. Garcia-Gonzalo FR, Reiter JF. 2012. Scoring a backstage pass: mechanisms of ciliogenesis and ciliary access. The Journal of Cell Biology 197:697-709. doi: 10.1083/jcb.201111146.
17. Geng L, Okuhara D, Yu Z, Tian X, Cai Y, Shibazaki S, Somlo S. 2006. Polycystin-2 traffics to cilia independently of polycystin-1 by using an N-terminal RVxP motif. Journal of Cell Science 119:1383-1395. doi: 10.1242/jcs.02818.
18. Gilula NB, Satir P. 1972. The ciliary necklace. The Journal of Cell Biology 53:494-509. doi: 10.1083/jcb.53.2.494.
19. Händel M, Schulz S, Stanarius A, Schreff M, Erdtmann-Vourliotis M, Schmidt H, Wolf G, Höllt V. 1999. Selective targeting of somatostatin receptor 3 to neuronal cilia. Neuroscience 89:909-926. doi: 10.1016/S0306-4522(98) 00354-6.
20. Hoffmeister H, Babinger K, Gürster S, Cedzich A, Meese C, Schadendorf K, Osten L, De Vries U, Rascle A, Witzgall R. 2011. Polycystin-2 takes different routes to the somatic and ciliary plasma membrane. Cell 1:631-645. doi: 10. 1083/jcb.201007050.
21. Howard PW, Jue SF, Maurer RA. 2013. Interaction of mouse TTC30/DYF-1 with multiple intraflagellar transport complex B proteins and KIF17. Experimental Cell Research 319:2275-2281. doi: 10.1016/j.yexcr.2013.06.010.
22. Hsiao Y, Tuz K, Ferland RJ. 2012. Trafficking in and to the primary cilium. Cilia 1:4. doi: 10.1186/2046-2530-1-4.
23. Hu Q, Milenkovic L, Jin H, Scott MP, V Nachury M, Spiliotis ET, Nelson WJ. 2010. A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 329:436-439. doi: 10.1126/ science.1191054.
24. Huang K, Diener DR, Mitchell A, Pazour GJ, Witman GB, Rosenbaum JL. 2007. Function and dynamics of PKD2 in Chlamydomonas reinhardtii flagella. The Journal of Cell Biology 179:501-514. doi: 10.1083/jcb.200704069.
25. Hunnicutt GR, Kosfiszer MG, Snell WJ. 1990. Cell body and flagellar agglutinins in Chlamydomonas reinhardtii: the cell body plasma membrane is a reservoir for agglutinins whose migration to the flagella is regulated by a functional barrier. The Journal of Cell Biology 111:1605-1616. doi: 10.1083/jcb.111.4.1605.
26. Insinna C, Pathak N, Perkins B, Drummond I, Besharse JC. 2008. The homodimeric kinesin, Kif17, is essential for vertebrate photoreceptor sensory outer segment development. Developmental Biology 316:160-170. doi: 10. 1016/j.ydbio.2008.01.025.
27. Jenkins PM, Hurd TW, Zhang L, McEwen DP, Brown RL, Margolis B, Verhey KJ, Martens JR. 2006. Ciliary targeting of olfactory CNG channels requires the CNGB1b subunit and the Kinesin-2 motor protein, KIF17. Current Biology 16:1211-1216. doi: 10.1016/j.cub.2006.04.034.
28. Jin H, White SR, Shida T, Schulz S, Aguiar M, Gygi SP, Bazan JF, Nachury MV. 2010. The conserved bardet-biedl syndrome proteins assemble a coat that traffics membrane proteins to Cilia. Cell 141:1208-1219. doi: 10.1016/j. cell.2010.05.015.
29. Keady BT, Le YZ, Pazour GJ. 2011. IFT20 is required for opsin trafficking and photoreceptor outer segment development. Molecular Biology of the Cell 22:921-930. doi: 10.1091/mbc.E10-09-0792.
30. Keady BT, Samtani R, Tobita K, Tsuchya M, Agustin JTS, Follit JA, Jonassen JA, Subramanian R, Lo CW, Pazour GJ. 2012. Article IFT25 links the signal-dependent movement of hedgehog components to intraflagellar transport. Developmental Cell 22:940-951. doi: 10.1016/j.devcel.2012.04.009.
31. Krock BL, Perkins BD. 2008. The intraflagellar transport protein IFT57 is required for cilia maintenance and regulates IFT-particle-kinesin-II dissociation in vertebrate photoreceptors. Journal of Cell Science 121: 1907-1915. doi: 10.1242/jcs.029397.
32. Kuzhandaivel A, Schultz SW, Alkhori L, Alenius M. 2014. Cilia-mediated hedgehog signaling in Drosophila. Cell Reports 7:672-680. doi: 10.1016/j.celrep.2014.03.052.
33. Lippincott-Schwartz J, Altan-Bonnet N, Patterson GH. 2003. Photobleaching and photoactivation: following protein dynamics in living cells. Nature Cell Biology (Suppl S7-S14).
34. Marley A, von Zastrow M. 2010. DISC1 regulates primary cilia that display specific dopamine receptors. PLOS ONE 5:e10902. doi: 10.1371/journal.pone.0010902.
35. Mazelova J, Ransom N, Astuto-Gribble L, Wilson MC, Deretic D. 2009. Syntaxin 3 and SNAP-25 pairing, regulated by omega-3 docosahexaenoic acid, controls the delivery of rhodopsin for the biogenesis of cilia-derived sensory organelles, the rod outer segments. Journal of Cell Science 122:2003-2013. doi: 10.1242/jcs.039982.
36. Milenkovic L, Scott MP, Rohatgi R. 2009. Lateral transport of smoothened from the plasma membrane to the membrane of the cilium. The Journal of Cell Biology 187:365-374. doi: 10.1083/jcb.200907126.
37. Mukhopadhyay S, Wen X, Chih B, Nelson CD, Lane WS, Scales SJ, Jackson PK. 2010. TULP3 bridges the IFT-A complex and membrane phosphoinositides to promote trafficking of G protein-coupled receptors into primary cilia. Genes & Development 24:2180-2193. doi: 10.1101/gad.1966210.
38. Mukhopadhyay S, Wen X, Ratti N, Loktev A, Rangell L, Scales SJ, Jackson PK. 2013. The ciliary G-protein-coupled receptor Gpr161 negatively regulates the sonic hedgehog pathway via cAMP signaling. Cell 152:210-223. doi: 10.1016/j.cell.2012.12.026.
39. Nachury MV, Loktev AV, Zhang Q, Westlake CJ, Peränen J, Merdes A, Slusarski DC, Scheller RH, Bazan JF, Sheffield VC, Jackson PK. 2007. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129:1201-1213. doi: 10.1016/j.cell.2007.03.053.
40. Pedersen LB, Rosenbaum JL. 2008. Chapter two intraflagellar transport (IFT): role in ciliary assembly, resorption and signalling. Current Topics in Developmental Biology 85:23-61. doi: 10.1016/S0070-2153(08)00802-8.
41. Rice S, Lin AW, Safer D, Hart CL, Naber N, Carragher BO, Cain SM, Pechatnikova E, Wilson-Kubalek EM, Whittaker M, Pate E, Cooke R, Taylor EW, Milligan RA, Vale RD. 1999. A structural change in the kinesin motor protein that drives motility. Nature 402:778-784. doi: 10.1038/45483.
42. Schulz S, Händel M, Schreff M, Schmidt H, Höllt V. 2000. Localization of five somatostatin receptors in the rat central nervous system using subtype-specific antibodies. Journal of Physiology 94:259-264. doi: 10.1016/S0928-4257(00)00212-6.
43. Silverman MA, Leroux MR. 2009. Intraflagellar transport and the generation of dynamic, structurally and functionally diverse cilia. Trends in Cell Biology 19:306-316. doi: 10.1016/j.tcb.2009.04.002.
44. Tanowitz M, Von Zastrow M. 2003. A novel endocytic recycling signal that distinguishes the membrane trafficking of naturally occurring opioid receptors. The Journal of Biological Chemistry 278:45978-45986. doi: 10.1074/jbc. M304504200.
45. Tsao PI, Von Zastrow M. 2000. Type-specific sorting of G protein-coupled receptors after endocytosis. The Journal of Biological Chemistry 275:11130-11140. doi: 10.1074/jbc.275.15.11130.
46. Vickery RG, von Zastrow M. 1999. Distinct dynamin-dependent and-independent mechanisms target structurally homologous dopamine receptors to different endocytic membranes. The Journal of Cell Biology 144:31-43. doi: 10.1083/jcb.144.1.31.
47. Wang J, Morita Y, Mazelova J, Deretic D. 2012. The Arf GAP ASAP1 provides a platform to ciliary receptor targeting. The EMBO Journal 31:4057-4071. doi: 10.1038/emboj.2012.253.
48. Wang Y, Zhou Z, Walsh CT, McMahon AP. 2009. Selective translocation of intracellular smoothened to the primary cilium in response to hedgehog pathway modulation. Proceedings of the National Academy of Sciences of USA 106:2623-2628. doi: 10.1073/pnas.0812110106.
49. Williams CL, Li C, Kida K, Inglis PN, Mohan S, Semenec L, Bialas NJ, Stupay RM, Chen N, Blacque OE, Yoder BK, Leroux MR. 2011. MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis. The Journal of Cell Biology 192:1023-1041. doi: 10. 1083/jcb.201012116.
50. Yu YJ, Dhavan R, Chevalier MW, Yudowski GA, von Zastrow M. 2010. Rapid delivery of internalized signaling receptors to the somatodendritic surface by sequence-specific local insertion. The Journal of Neuroscience 30: 11703-11714. doi: 10.1523/JNEUROSCI.6282-09.2010.
51. Zhang Q, Nishimura D, Vogel T, Shao J, Swiderski R, Yin T, Searby C, Carter CS, Kim G, Bugge K, Stone EM, Sheffield VC. 2013. BBS7 is required for BBSome formation and its absence in mice results in Bardet-Biedl syndrome phenotypes and selective abnormalities in membrane protein trafficking. Journal of Cell Science 126: 2372-2380. doi: 10.1242/jcs.111740.
52. Zhao C, Omori Y, Brodowska K, Kovach P, Malicki J. 2012. Kinesin-2 family in vertebrate ciliogenesis. Proceedings of the National Academy of Sciences of USA 109:2388-2393. doi: 10.1073/pnas.1116035109.