Recruitment of β-arrestin into neuronal cilia modulates somatostatin receptor subtype 3 ciliary localization

Molecular and Cellular Biology

Volumn 36, Issue 1, 2016, Pages 223-235

  Green, Jill A ^a   Schmid, Cullen L ^b   Bley, Elizabeth ^a   Monsma, Paula C ^a   Brown, Anthony ^a   Bohn, Laura M ^b   Mykytyn, Kirk ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ARRESTIN; RETINA S ANTIGEN; SOMATOSTATIN; SOMATOSTATIN RECEPTOR 3; ARRB2 PROTEIN, HUMAN; ARRB2 PROTEIN, MOUSE; BETA ARRESTIN 2; SOMATOSTATIN RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; CENTRIOLE; CILIARY BODY; CILIARY MOTILITY; CONTROLLED STUDY; DIMERIZATION; EUKARYOTIC FLAGELLUM; GENETIC TRANSFECTION; INTERNALIZATION; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; ANIMAL; BRAIN; CELL CULTURE; LEARNING; MEMORY; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ARRESTINS; BETA-ARRESTIN 2; BETA-ARRESTINS; BRAIN; CELLS, CULTURED; CILIA; LEARNING; MEMORY; MICE; NEURONS; RECEPTORS, SOMATOSTATIN; SIGNAL TRANSDUCTION;

EID: 84954183498     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00765-15     Document Type: Article

References (62)

1. Berbari NF, O'Connor AK, Haycraft CJ, Yoder BK. 2009. The primary cilium as a complex signaling center. Curr Biol 19:R526-R535. http://dx.doi.org/10.1016/j.cub.2009.05.025.
2. Green JA, Mykytyn K. 2010. Neuronal ciliary signaling in homeostasis and disease. Cell Mol Life Sci 67:3287-3297. http://dx.doi.org/10.1007/s00018-010-0425-4.
3. Satir P, Pedersen LB, Christensen ST. 2010. The primary cilium at a glance. J Cell Sci 123:499-503. http://dx.doi.org/10.1242/jcs.050377.
4. Goetz SC, Anderson KV. 2010. The primary cilium: a signalling centre during vertebrate development. Nat Rev Genet 11:331-344. http://dx.doi.org/10.1038/nrg2774.
5. Lienkamp S, Ganner A, Walz G. 2012. Inversin, Wnt signaling and primary cilia. Differentiation 83:S49-S55. http://dx.doi.org/10.1016/j.diff.2011.11.012.
6. Schou KB, Pedersen LB, Christensen ST. 2015. Ins and outs of GPCR signaling in primary cilia. EMBO Rep 16:1099-1113. http://dx.doi.org/10.15252/embr.201540530.
7. Hildebrandt F, Benzing T, Katsanis N. 2011. Ciliopathies. N Engl J Med 364:1533-1543. http://dx.doi.org/10.1056/NEJMra1010172.
8. Garcia-Gonzalo FR, Reiter JF. 2012. Scoring a backstage pass: mechanisms of ciliogenesis and ciliary access. J Cell Biol 197:697-709. http://dx.doi.org/10.1083/jcb.201111146.
9. Nachury MV, Seeley ES, Jin H. 2010. Trafficking to the ciliary membrane: how to get across the periciliary diffusion barrier? Annu Rev Cell Dev Biol 26:59-87. http://dx.doi.org/10.1146/annurev.cellbio.042308.113337.
10. Berbari NF, Lewis JS, Bishop GA, Askwith CC, Mykytyn K. 2008. Bardet-Biedl syndrome proteins are required for the localization of G protein-coupled receptors to primary cilia. Proc Natl Acad Sci U S A 105:4242-4246. http://dx.doi.org/10.1073/pnas.0711027105.
11. Garcia-Gonzalo FR, Corbit KC, Sirerol-Piquer MS, Ramaswami G, Otto EA, Noriega TR, Seol AD, Robinson JF, Bennett CL, Josifova DJ, Garcia-Verdugo JM, Katsanis N, Hildebrandt F, Reiter JF. 2011. A transition zone complex regulates mammalian ciliogenesis and ciliary membrane composition. Nat Genet 43:776-784. http://dx.doi.org/10.1038/ng.891.
12. McEwen DP, Koenekoop RK, Khanna H, Jenkins PM, Lopez I, Swaroop A, Martens JR. 2007. Hypomorphic CEP290/NPHP6 mutations result in anosmia caused by the selective loss of G proteins in cilia of olfactory sensory neurons. Proc Natl Acad Sci USA 104:15917-15922. http://dx.doi.org/10.1073/pnas.0704140104.
13. Corbit KC, Aanstad P, Singla V, Norman AR, Stainier DY, Reiter JF. 2005. Vertebrate Smoothened functions at the primary cilium. Nature 437:1018-1021. http://dx.doi.org/10.1038/nature04117.
14. Haycraft CJ, Banizs B, Aydin-Son Y, Zhang Q, Michaud EJ, Yoder BK. 2005. Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein Polaris for processing and function. PLoS Genet 1:e53. http://dx.doi.org/10.1371/journal.pgen.0010053.
15. Kim J, Kato M, Beachy PA. 2009. Gli2 trafficking links Hedgehogdependent activation of Smoothened in the primary cilium to transcriptional activation in the nucleus. Proc Natl Acad Sci U S A 106:21666-21671. http://dx.doi.org/10.1073/pnas.0912180106.
16. Rohatgi R, Milenkovic L, Scott MP. 2007. Patched1 regulates Hedgehog signaling at the primary cilium. Science 317:372-376. http://dx.doi.org/10.1126/science.1139740.
17. Najafi M, Calvert PD. 2012. Transport and localization of signaling proteins in ciliated cells. Vision Res 75:11-18. http://dx.doi.org/10.1016/j.visres.2012.08.006.
18. Handel M, Schulz S, Stanarius A, Schreff M, Erdtmann-Vourliotis M, Schmidt H, Wolf G, Hollt V. 1999. Selective targeting of somatostatin receptor 3 to neuronal cilia. Neuroscience 89:909-926. http://dx.doi.org/10.1016/S0306-4522(98)00354-6.
19. Brailov I, Bancila M, Brisorgueil MJ, Miquel MC, Hamon M, Verge D. 2000. Localization of 5-HT(6) receptors at the plasma membrane of neuronal cilia in the rat brain. Brain Res 872:271-275. http://dx.doi.org/10.1016/S0006-8993(00)02519-1.
20. Hamon M, Doucet E, Lefevre K, Miquel MC, Lanfumey L, Insausti R, Frechilla D, Del Rio J, Verge D. 1999. Antibodies and antisense oligonucleotide for probing the distribution and putative functions of central 5-HT6 receptors. Neuropsychopharmacology 21:68S-76S. http://dx.doi.org/10.1038/sj.npp.1395368.
21. Berbari NF, Johnson AD, Lewis JS, Askwith CC, Mykytyn K. 2008. Identification of ciliary localization sequences within the third intracellular loop of G protein-coupled receptors. Mol Biol Cell 19:1540-1547. http://dx.doi.org/10.1091/mbc.E07-09-0942.
22. Domire JS, Green JA, Lee KG, Johnson AD, Askwith CC, Mykytyn K. 2011. Dopamine receptor 1 localizes to neuronal cilia in a dynamic process that requires the Bardet-Biedl syndrome proteins. Cell Mol Life Sci 68:2951-2960. http://dx.doi.org/10.1007/s00018-010-0603-4.
23. Soetedjo L, Glover DA, Jin H. 2013. Targeting of vasoactive intestinal peptide receptor 2, VPAC2, a secretin family G-protein coupled receptor, to primary cilia. Biol Open 2:686-694. http://dx.doi.org/10.1242/bio.20134747.
24. Loktev AV, Jackson PK. 2013. Neuropeptide Y family receptors traffic via the Bardet-Biedl syndrome pathway to signal in neuronal primary cilia. Cell Rep 5:1316-1329. http://dx.doi.org/10.1016/j.celrep.2013.11.011.
25. Koemeter-Cox AI, Sherwood TW, Green JA, Steiner RA, Berbari NF, Yoder BK, Kauffman AS, Monsma PC, Brown A, Askwith CC, Mykytyn K. 2014. Primary cilia enhance kisspeptin receptor signaling on gonadotropin-releasing hormone neurons. Proc Natl Acad Sci U S A 111:10335-10340. http://dx.doi.org/10.1073/pnas.1403286111.
26. Bishop GA, Berbari NF, Lewis JS, Mykytyn K. 2007. Type III adenylyl cyclase localizes to primary cilia throughout the adult mouse brain. J Comp Neurol 505:562-571. http://dx.doi.org/10.1002/cne.21510.
27. Hanyaloglu AC, von Zastrow M. 2008. Regulation of GPCRs by endocytic membrane trafficking and its potential implications. Annu Rev Pharmacol Toxicol 48:537-568. http://dx.doi.org/10.1146/annurev.pharmtox.48.113006.094830.
28. Marchese A, Paing MM, Temple BR, Trejo J. 2008. G protein-coupled receptor sorting to endosomes and lysosomes. Annu Rev Pharmacol Toxicol 48:601-629. http://dx.doi.org/10.1146/annurev.pharmtox.48.113006.094646.
29. Kelly E, Bailey CP, Henderson G. 2008. Agonist-selective mechanisms of GPCR desensitization. Br J Pharmacol 153(Suppl 1):S379-S388.
30. Shenoy SK, Lefkowitz RJ. 2011. beta-Arrestin-mediated receptor trafficking and signal transduction. Trends Pharmacol Sci 32:521-533. http://dx.doi.org/10.1016/j.tips.2011.05.002.
31. Shukla AK, Xiao K, Lefkowitz RJ. 2011. Emerging paradigms of betaarrestin-dependent seven transmembrane receptor signaling. Trends Biochem Sci 36:457-469. http://dx.doi.org/10.1016/j.tibs.2011.06.003.
32. Dawson TM, Arriza JL, Jaworsky DE, Borisy FF, Attramadal H, Lefkowitz RJ, Ronnett GV. 1993. Beta-adrenergic receptor kinase-2 and betaarrestin-2 as mediators of odorant-induced desensitization. Science 259:825-829. http://dx.doi.org/10.1126/science.8381559.
33. 2+/calmodulin-dependent protein kinase II and phosphodiesterase PDE1C2, and a Cl(-)-cotransporter in rodent olfactory epithelia. J Neurocytol 34:11-36. http://dx.doi.org/10.1007/s11068-005-5045-9.
34. Kovacs JJ, Whalen EJ, Liu R, Xiao K, Kim J, Chen M, Wang J, Chen W, Lefkowitz RJ. 2008. Beta-arrestin-mediated localization of Smoothened to the primary cilium. Science 320:1777-1781. http://dx.doi.org/10.1126/science.1157983.
35. Molla-Herman A, Boularan C, Ghossoub R, Scott MG, Burtey A, Zarka M, Saunier S, Concordet JP, Marullo S, Benmerah A. 2008. Targeting of beta-arrestin2 to the centrosome and primary cilium: role in cell proliferation control. PLoS One 3:e3728. http://dx.doi.org/10.1371/journal.pone.0003728.
36. Bohn LM, Lefkowitz RJ, Gainetdinov RR, Peppel K, Caron MG, Lin FT. 1999. Enhanced morphine analgesia in mice lacking beta-arrestin 2. Science 286:2495-2498. http://dx.doi.org/10.1126/science.286.5449.2495.
37. Barak LS, Ferguson SS, Zhang J, Caron MG. 1997. A beta-arrestin/green fluorescent protein biosensor for detecting G protein-coupled receptor activation. J Biol Chem 272:27497-27500. http://dx.doi.org/10.1074/jbc.272.44.27497.
38. Barak LS, Warabi K, Feng X, Caron MG, Kwatra MM. 1999. Real-time visualization of the cellular redistribution of G protein-coupled receptor kinase 2 and beta-arrestin 2 during homologous desensitization of the substance P receptor. J Biol Chem 274:7565-7569. http://dx.doi.org/10.1074/jbc.274.11.7565.
39. Domire JS, Mykytyn K. 2009. Markers for neuronal cilia. Methods Cell Biol 91:111-121. http://dx.doi.org/10.1016/S0091-679X(08)91006-2.
40. Berbari NF, Bishop GA, Askwith CC, Lewis JS, Mykytyn K. 2007. Hippocampal neurons possess primary cilia in culture. J Neurosci Res 85:1095-1100. http://dx.doi.org/10.1002/jnr.21209.
41. Green JA, Gu C, Mykytyn K. 2012. Heteromerization of ciliary G protein-coupled receptors in the mouse brain. PLoS One 7:e46304. http://dx.doi.org/10.1371/journal.pone.0046304.
42. Kreuzer OJ, Krisch B, Dery O, Bunnett NW, Meyerhof W. 2001. Agonist-mediated endocytosis of rat somatostatin receptor subtype 3 involves beta-arrestin and clathrin coated vesicles. J Neuroendocrinol 13:279-287.
43. Breslow DK, Koslover EF, Seydel F, Spakowitz AJ, Nachury MV. 2013. An in vitro assay for entry into cilia reveals unique properties of the soluble diffusion barrier. J Cell Biol 203:129-147. http://dx.doi.org/10.1083/jcb.201212024.
44. Schafer J, Baumeister H, Meyerhof W, Nehring R, Richter D. 1996. Characterization of cloned somatostatin receptor subtypes. Localization of rat SSTRs in gastrointestinal tissues, SSTR1 gene promoter studies, and mutational analyses of SSTR3. Ann N Y Acad Sci 805:601-606.
45. Roth A, Kreienkamp HJ, Meyerhof W, Richter D. 1997. Phosphorylation of four amino acid residues in the carboxyl terminus of the rat somatostatin receptor subtype 3 is crucial for its desensitization and internalization. J Biol Chem 272:23769-23774. http://dx.doi.org/10.1074/jbc.272.38.23769.
46. Kee HL, Dishinger JF, Blasius TL, Liu CJ, Margolis B, Verhey KJ. 2012. A size-exclusion permeability barrier and nucleoporins characterize a ciliary pore complex that regulates transport into cilia. Nat Cell Biol 14:431-437. http://dx.doi.org/10.1038/ncb2450.
47. Lin YC, Niewiadomski P, Lin B, Nakamura H, Phua SC, Jiao J, Levchenko A, Inoue T, Rohatgi R. 2013. Chemically inducible diffusion trap at cilia reveals molecular sieve-like barrier. Nat Chem Biol 9:437-443. http://dx.doi.org/10.1038/nchembio.1252.
48. Komatsu T, Kukelyansky I, McCaffery JM, Ueno T, Varela LC, Inoue T. 2010. Organelle-specific, rapid induction of molecular activities and membrane tethering. Nat Methods 7:206-208. http://dx.doi.org/10.1038/nmeth.1428.
49. DeFea KA. 2011. Beta-arrestins as regulators of signal termination and transduction: how do they determine what to scaffold? Cell Signal 23:621-629. http://dx.doi.org/10.1016/j.cellsig.2010.10.004.
50. Benmerah A. 2013. The ciliary pocket. Curr Opin Cell Biol 25:78-84. http://dx.doi.org/10.1016/j.ceb.2012.10.011.
51. Rohatgi R, Snell WJ. 2010. The ciliary membrane. Curr Opin Cell Biol 22:541-546. http://dx.doi.org/10.1016/j.ceb.2010.03.010.
52. Molla-Herman A, Ghossoub R, Blisnick T, Meunier A, Serres C, Silbermann F, Emmerson C, Romeo K, Bourdoncle P, Schmitt A, Saunier S, Spassky N, Bastin P, Benmerah A. 2010. The ciliary pocket: an endocytic membrane domain at the base of primary and motile cilia. J Cell Sci 123:1785-1795. http://dx.doi.org/10.1242/jcs.059519.
53. Rattner JB, Sciore P, Ou Y, van der Hoorn FA, Lo IK. 2010. Primary cilia in fibroblast-like type B synoviocytes lie within a cilium pit: a site of endocytosis. Histol Histopathol 25:865-875.
54. McMahon HT, Boucrot E. 2011. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol 12:517-533. http://dx.doi.org/10.1038/nrm3151.
55. Sorkin A, von Zastrow M. 2009. Endocytosis and signalling: intertwining molecular networks. Nat Rev Mol Cell Biol 10:609-622. http://dx.doi.org/10.1038/nrm2748.
56. Kotowski SJ, Hopf FW, Seif T, Bonci A, von Zastrow M. 2011. Endocytosis promotes rapid dopaminergic signaling. Neuron 71:278-290. http://dx.doi.org/10.1016/j.neuron.2011.05.036.
57. Irannejad R, Tomshine JC, Tomshine JR, Chevalier M, Mahoney JP, Steyaert J, Rasmussen SG, Sunahara RK, El-Samad H, Huang B, von Zastrow M. 2013. Conformational biosensors reveal GPCR signalling from endosomes. Nature 495:534-538. http://dx.doi.org/10.1038/nature12000.
58. Clement CA, Ajbro KD, Koefoed K, Vestergaard ML, Veland IR, Henriques de Jesus MP, Pedersen LB, Benmerah A, Andersen CY, Larsen LA, Christensen ST. 2013. TGF-beta signaling is associated with endocytosis at the pocket region of the primary cilium. Cell Rep 3:1806-1814. http://dx.doi.org/10.1016/j.celrep.2013.05.020.
59. Najafi M, Maza NA, Calvert PD. 2012. Steric volume exclusion sets soluble protein concentrations in photoreceptor sensory cilia. Proc Natl Acad Sci U S A 109:203-208. http://dx.doi.org/10.1073/pnas.1115109109.
60. Pedersen LB, Rosenbaum JL. 2008. Intraflagellar transport (IFT) role in ciliary assembly, resorption and signalling. Curr Top Dev Biol 85:23-61. http://dx.doi.org/10.1016/S0070-2153(08)00802-8.
61. Ye F, Breslow DK, Koslover EF, Spakowitz AJ, Nelson WJ, Nachury MV. 2013. Single molecule imaging reveals a major role for diffusion in the exploration of ciliary space by signaling receptors. eLife 2:e00654. http://dx.doi.org/10.7554/eLife.00654.
62. Tulipano G, Stumm R, Pfeiffer M, Kreienkamp HJ, Hollt V, Schulz S. 2004. Differential beta-arrestin trafficking and endosomal sorting of somatostatin receptor subtypes. J Biol Chem 279:21374-21382. http://dx.doi.org/10.1074/jbc.M313522200.