Identification of ciliary localization sequences within the third intracellular loop of G protein-coupled receptors

Molecular Biology of the Cell

Volumn 19, Issue 4, 2008, Pages 1540-1547

  Berbari, Nicolas F ^a   Johnson, Andrew D ^a   Lewis, Jacqueline S ^a   Askwith, Candice C ^a   Mykytyn, Kirk ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; MELANIN CONCENTRATING HORMONE RECEPTOR 1; SEROTONIN 6 RECEPTOR; SEROTONIN 7 RECEPTOR; SOMATOSTATIN RECEPTOR 3; SOMATOSTATIN RECEPTOR 5;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL LINE; CILIA; CONSENSUS SEQUENCE; GREEN FLUORESCENT PROTEINS; HUMANS; KIDNEY TUBULES, COLLECTING; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, SEROTONIN; RECEPTORS, SOMATOSTATIN; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

MAMMALIA;

EID: 44449106038     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-09-0942     Document Type: Article

References (50)

1. Badano, J. L., Mitsuma, N., Beales, P. L., and Katsanis, N. (2006). The ciliopathies: an emerging class of human genetic disorders. Annu. Rev. Genomics Hum. Genet. 7, 125-148.
2. Berbari, N. F., Bishop, G. A., Askwith, C. C., Lewis, J. S., and Mykytyn, K. (2007). Hippocampal neurons possess primary cilia in culture. J. Neurosci. Res. 85, 1095-1100.
3. Bisgrove, B. W., and Yost, H. J. (2006). The roles of cilia in developmental disorders and disease. Development 133, 4131-4143.
4. Bishop, G. A., Berbari, N. F., Lewis, J. S., and Mykytyn, K. (2007). Type III adenylyl cyclase localizes to primary cilia throughout the adult mouse brain. J. Comp. Neurol. 505, 562-571.
5. Bloodgood, R. A. (2000). Protein targeting to flagella of trypanosomatid protozoa. Cell Biol. Int. 24, 857-862.
6. Borowsky, B. et al. (2002). Antidepressant, anxiolytic and anorectic effects of a melanin-concentrating hormone-1 receptor antagonist. Nat. Med. 8, 825-830.
7. Brailov, I., Bancila, M., Brisorgueil, M. J., Miquel, M. C., Hamon, M., and 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.
8. Chen, Y. et al. (2002). Targeted disruption of the melanin-concentrating hormone receptor-1 results in hyperphagia and resistance to diet-induced obesity. Endocrinology 143, 2469-2477.
9. Corbit, K. C., Aanstad, P., Singla, V., Norman, A. R., Stainier, D. Y., and Reiter, J. F. (2005). Vertebrate Smoothened functions at the primary cilium. Nature 437, 1018-1021.
10. Davenport, J. R., Watts, A. J., Roper, V. C., Croyle, M. J., van Groen, T., Wyss, J. M., Nagy, T. R., Kesterson, R. A., and Yoder, B. K. (2007). Disruption of intraflagellar transport in adult mice leads to obesity and slow-onset cystic kidney disease. Curr. Biol. 17, 1586-1594.
11. Davenport, J. R., and Yoder, B. K. (2005). An incredible decade for the primary cilium: a look at a once-forgotten organelle. Am. J. Physiol. Renal. Physiol. 289, F1159-F1169.
12. Deretic, D., Schmerl, S., Hargrave, P. A., Arendt, A., and McDowell, J. H. (1998). Regulation of sorting and post-Golgi trafficking of rhodopsin by its C-terminal sequence QVS(A)PA. Proc. Natl. Acad. Sci. USA 95, 10620-10625.
13. Dong, C., Filipeanu, C. M., Duvernay, M. T., and Wu, G. (2007). Regulation of G protein-coupled receptor export trafficking. Biochim. Biophys. Acta 1768, 853-870.
14. Dwyer, N. D., Adler, C. E., Crump, J. G., L'Etoile, N. D., and Bargmann, C. I. (2001). Polarized dendritic transport and the AP-1 mu1 clathrin adaptor UNC-101 localize odorant receptors to olfactory cilia. Neuron 31, 277-287.
15. Egan, C. T., Herrick-Davis, K., and Teitler, M. (1998). Creation of a constitutively activated state of the 5-hydroxytryptamine2A receptor by site-directed mutagenesis: inverse agonist activity of antipsychotic drugs. J. Pharmacol. Exp. Ther. 286, 85-90.
16. Gelber, E. I., Kroeze, W. K., Willins, D. L., Gray, J. A., Sinar, C. A., Hyde, E. G., Gurevich, V., Benovic, J., and Roth, B. L. (1999). Structure and function of the third intracellular loop of the 5-hydroxytryptamine2A receptor: the third intracellular loop is alpha-helical and binds purified arrestins. J. Neurochem. 72, 2206-2214.
17. Geng, L., Okuhara, D., Yu, Z., Tian, X., Cai, Y., Shibazaki, S., and Somlo, S. (2006). Polycystin-2 traffics to cilia independently of polycystin-1 by using an N-terminal RVxP motif. J. Cell Sci. 119, 1383-1395.
18. Gonnet, G. H., Cohen, M. A., and Benner, S. A. (1992). Exhaustive matching of the entire protein sequence database. Science 256, 1443-1445.
19. Hamon, M., Doucet, E., Lefevre, K., Miquel, M. C., Lanfumey, L., Insausti, R., Frechilla, D., Del Rio, J., and Verge, D. (1999). Antibodies and antisense oligonucleotide for probing the distribution and putative functions of central 5-HT6 receptors. Neuropsychopharmacology 21, 68S-76S.
20. Handel, M., Schulz, S., Stanarius, A., Schreff, M., Erdtmann-Vourliotis, M., Schmidt, H., Wolf, G., and Hollt, V. (1999). Selective targeting of somatostatin receptor 3 to neuronal cilia. Neuroscience 89, 909-926.
21. Hermosilla, R., and Schulein, R. (2001). Sorting functions of the individual cytoplasmic domains of the G protein-coupled vasopressin V(2) receptor in Madin Darby canine kidney epithelial cells. Mol. Pharmacol. 60, 1031-1039.
22. Hildebrandt, F., and Otto, E. (2005). Cilia and centrosomes: a unifying pathogenic concept for cystic kidney disease? Nat. Rev. Genet. 6, 928-940.
23. Hipkin, R. W., Wang, Y., and Schonbrunn, A. (2000). Protein kinase C activation stimulates the phosphorylation and internalization of the sst2A somatostatin receptor. J. Biol. Chem. 275, 5591-5599.
24. Horn, F., Bettler, E., Oliveira, L., Campagne, F., Cohen, F. E., and Vriend, G. (2003). GPCRDB information system for G protein-coupled receptors. Nucleic Acids Res. 31, 294-297.
25. Horton, R. M., Cai, Z. L., Ho, S. N., and Pease, L. R. (1990). Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8, 528-535.
26. Hu, J., Bae, Y. K., Knobel, K. M., and Barr, M. M. (2006). Casein kinase II and calcineurin modulate TRPP function and ciliary localization. Mol. Biol. Cell 17, 2200-2211.
27. Jenkins, P. M., Hurd, T. W., Zhang, L., McEwen, D. P., Brown, R. L., Margolis, B., Verhey, K. J., and Martens, J. R. (2006). Ciliary targeting of olfactory CNG channels requires the CNGB1b subunit and the kinesin-2 motor protein, KIF17. Curr. Biol. 16, 1211-1216.
28. Kjelsberg, M. A., Cotecchia, S., Ostrowski, J., Caron, M. G., and Lefkowitz, R. J. (1992). Constitutive activation of the alpha 1B-adrenergic receptor by all amino acid substitutions at a single site. Evidence for a region which constrains receptor activation. J. Biol. Chem. 267, 1430-1433.
29. Kohen, R., Fashingbauer, L. A., Heidmann, D. E., Guthrie, C. R., and Hamblin, M. W. (2001). Cloning of the mouse 5-HT6 serotonin receptor and mutagenesis studies of the third cytoplasmic loop. Brain Res. Mol. Brain Res. 90, 110-117.
30. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E. L. (2001). Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580.
31. Ludwig, D. S., Tritos, N. A., Mastaitis, J. W., Kulkarni, R., Kokkotou, E., Elmquist, J., Lowell, B., Flier, J. S., and Maratos-Flier, E. (2001). Melanin-concentrating hormone overexpression in transgenic mice leads to obesity and insulin resistance. J. Clin. Invest 107, 379-386.
32. Marshall, W. F., and Nonaka, S. (2006). Cilia: tuning in to the cell's antenna. Curr. Biol. 16, R604-614.
33. Marszalek, J. R., Liu, X., Roberts, E. A., Chui, D., Marth, J. D., Williams, D. S., and Goldstein, L. S. (2000). Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors. Cell 102, 175-187.
34. McEwen, D. P., Koenekoop, R. K., Khanna, H., Jenkins, P. M., Lopez, I., Swaroop, A., and Martens, J. R. (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.
35. Nauli, S. M. et al. (2003). Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat. Genet. 33, 129-137.
36. Oksenberg, D., Havlik, S., Peroutka, S. J., and Ashkenazi, A. (1995). The third intracellular loop of the 5-hydroxytryptamine2A receptor determines effector coupling specificity. J. Neurochem. 64, 1440-1447.
37. Pan, J., Wang, Q., and Snell, W. J. (2005). Cilium-generated signaling and cilia-related disorders. Lab. Invest. 85, 452-463.
38. Patel, Y. C. (1999). Somatostatin and its receptor family. Front. Neuroendocrinol. 20, 157-198.
39. Pazour, G. J., and Witman, G. B. (2003). The vertebrate primary cilium is a sensory organelle. Curr. Opin. Cell Biol. 15, 105-110.
40. Pissios, P., Bradley, R. L., and Maratos-Flier, E. (2006). Expanding the scales: the multiple roles of MCH in regulating energy balance and other biological functions. Endocr. Rev. 27, 606-620.
41. Praetorius, H. A., and Spring, K. R. (2001). Bending the MDCK cell primary cilium increases intracellular calcium. J. Membr. Biol. 184, 71-79.
42. Qin, H., Burnette, D. T., Bae, Y. K., Forscher, P., Barr, M. M., and Rosenbaum, J. L. (2005). Intraflagellar transport is required for the vectorial movement of TRPV channels in the ciliary membrane. Curr. Biol. 15, 1695-1699.
43. Qu, D., Ludwig, D. S., Gammeltoft, S., Piper, M., Pelleymounter, M. A., Cullen, M. J., Mathes, W. F., Przypek, R., Kanarek, R., and Maratos-Flier, E. (1996). A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 380, 243-247.
44. Ren, Q., Kurose, H., Lefkowitz, R. J., and Cotecchia, S. (1993). Constitutively active mutants of the alpha 2-adrenergic receptor. J. Biol. Chem. 268, 16483-16487.
45. Rosenbaum, J. L., and Witman, G. B. (2002). Intraflagellar transport. Nat. Rev. Mol. Cell Biol. 3, 813-825.
46. Schulz, S., Handel, M., Schreff, M., Schmidt, H., and Hollt, V. (2000). Localization of five somatostatin receptors in the rat central nervous system using subtype-specific antibodies. J. Physiol. Paris 94, 259-264.
47. Shimada, M., Tritos, N. A., Lowell, B. B., Flier, J. S., and Maratos-Flier, E. (1998). Mice lacking melanin-concentrating hormone are hypophagic and lean. Nature 396, 670-674.
48. Singla, V., and Reiter, J. F. (2006). The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 313, 629-633.
49. Takeda, S., Kadowaki, S., Haga, T., Takaesu, H., and Mitaku, S. (2002). Identification of G protein-coupled receptor genes from the human genome sequence. FEBS Lett. 520, 97-101.
50. Wheatley, D. N., Wang, A. M., and Strugnell, G. E. (1996). Expression of primary cilia in mammalian cells. Cell Biol. Int. 20, 73-81.