A Membrane-proximal, C-terminal α-Helix Is required for Plasma membrane localization and function of the G Protein-coupled Receptor (GPCR) TGR5

Journal of Biological Chemistry

Volumn 289, Issue 6, 2014, Pages 3689-3702

  Spomer, Lina ^a   Gertzen, Christoph G W ^a   Schmitz, Birte ^a   Häussinger, Dieter ^a   Gohlke, Holger ^a   Keitel, Verena ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

7-HELIX RECEPTOR; BILE ACID; CYCLIC AMP (CAMP); MOLECULAR DYNAMICS; TRAFFICKING;

CELL MEMBRANE; ENDOPLASMIC RETICULUM; HEK293 CELLS; HUMANS; PEPTIDES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTORS, ADRENERGIC, BETA-2; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, LYSOSPHINGOLIPID; RECEPTORS, OPIOID, KAPPA;

EID: 84893696729     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.502344     Document Type: Article

References (56)

1. Kawamata, Y., Fujii, R., Hosoya, M., Harada, M., Yoshida, H., Miwa, M., Fukusumi, S., Habata, Y., Itoh, T., Shintani, Y., Hinuma, S., Fujisawa, Y., and Fujino, M. (2003) A G protein-coupled receptor responsive to bile acids. J. Biol. Chem. 278, 9435-9440
2. Maruyama, T., Miyamoto, Y., Nakamura, T., Tamai, Y., Okada, H., Sugiyama, E., Nakamura, T., Itadani, H., and Tanaka, K. (2002) Identifica-tion of membrane-type receptor for bile acids (M-BAR). Biochem. Biophys. Res. Commun. 298, 714-719
3. Maruyama, T., Tanaka, K., Suzuki, J., Miyoshi, H., Harada, N., Nakamura, T., Miyamoto, Y., Kanatani, A., and Tamai, Y. (2006) Targeted disruption of G protein-coupled bile acid receptor 1 (Gpbar1/M-Bar) in mice. J. Endocrinol. 191, 197-205
4. Vassileva, G., Golovko, A., Markowitz, L., Abbondanzo, S. J., Zeng, M., Yang, S., Hoos, L., Tetzloff, G., Levitan, D., Murgolo, N. J., Keane, K., Davis, H. R., Jr., Hedrick, J., and Gustafson, E. L. (2006) Targeted deletion of Gpbar1 protects mice from cholesterol gallstone formation. Biochem. J. 398, 423-430
5. Keitel, V., Görg, B., Bidmon, H. J., Zemtsova, I., Spomer, L., Zilles, K., and Häussinger, D. (2010) The bile acid receptor TGR5 (Gpbar-1) acts as a neurosteroid receptor in brain. Glia 58, 1794-1805
6. Sato, H., Macchiarulo, A., Thomas, C., Gioiello, A., Une, M., Hofmann, A. F., Saladin, R., Schoonjans, K., Pellicciari, R., and Auwerx, J. (2008) Novel potent and selective bile acid derivatives as TGR5 agonists. Biological screening, structure-Activity relationships, and molecular modeling studies. J. Med. Chem. 51, 1831-1841
7. Keitel, V., and Häussinger, D. (2012) Perspective. TGR5 (Gpbar-1) in liver physiology and disease. Clin. Res. Hepatol. Gastroenterol. 36, 412-419
8. Keitel, V., Donner, M., Winandy, S., Kubitz, R., and Häussinger, D. (2008) Expression and function of the bile acid receptor TGR5 in Kupffer cells. Biochem. Biophys. Res. Commun. 372, 78-84
9. Keitel, V., Reinehr, R., Gatsios, P., Rupprecht, C., Görg, B., Selbach, O., Häussinger, D., and Kubitz, R. (2007) The G-protein coupled bile salt receptor TGR5 is expressed in liver sinusoidal endothelial cells. Hepatology 45, 695-704
10. Keitel, V., Cupisti, K., Ullmer, C., Knoefel, W. T., Kubitz, R., and Häussinger, D. (2009) The membrane-bound bile acid receptor TGR5 is localized in the epithelium of human gallbladders. Hepatology 50, 861-870
11. Keitel, V., Ullmer, C., and Häussinger, D. (2010) The membrane-bound bile acid receptor TGR5 (Gpbar-1) is localized in the primary cilium of cholangiocytes. Biol. Chem. 391, 785-789
12. Lavoie, B., Balemba, O. B., Godfrey, C., Watson, C. A., Vassileva, G., Corvera, C. U., Nelson, M. T., and Mawe, G. M. (2010) Hydrophobic bile salts inhibit gallbladder smooth muscle function via stimulation of GPBAR1 receptors and activation of KATP channels. J. Physiol. 588, 3295-3305
13. Li, T., Holmstrom, S. R., Kir, S., Umetani, M., Schmidt, D. R., Kliewer, S. A., and Mangelsdorf, D. J. (2011) The G protein-coupled bile acid receptor, TGR5, stimulates gallbladder filling. Mol. Endocrinol. 25, 1066-1071
14. Pols, T. W., Nomura, M., Harach, T., Lo Sasso, G., Oosterveer, M. H., Thomas, C., Rizzo, G., Gioiello, A., Adorini, L., Pellicciari, R., Auwerx, J., and Schoonjans, K. (2011) TGR5 activation inhibits atherosclerosis by reducing macrophage inflammation and lipid loading. Cell Metab. 14, 747-757
15. Wang, Y. D., Chen, W. D., Yu, D., Forman, B. M., and Huang, W. (2011) The G-Protein-coupled bile acid receptor, Gpbar1 (TGR5), negatively regulates hepatic inflammatory response through antagonizing nuclear factor-light-chain enhancer of activated B cells (NF-B) in mice. Hepatology 54, 1421-1432
16. Poole, D. P., Godfrey, C., Cattaruzza, F., Cottrell, G. S., Kirkland, J. G., Pelayo, J. C., Bunnett, N. W., and Corvera, C. U. (2010) Expression and function of the bile acid receptor GpBAR1 (TGR5) in the murine enteric nervous system. Neurogastroenterol. Motil. 22, 814-825
17. Reimann, F., Habib, A. M., Tolhurst, G., Parker, H. E., Rogers, G. J., and Gribble, F. M. (2008) Glucose sensing in L cells. A primary cell study. Cell Metab. 8, 532-539
18. Thomas, C., Gioiello, A., Noriega, L., Strehle, A., Oury, J., Rizzo, G., Macchiarulo, A., Yamamoto, H., Mataki, C., Pruzanski, M., Pellicciari, R., Auwerx, J., and Schoonjans, K. (2009) TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab. 10, 167-177
19. Pols, T. W., Noriega, L. G., Nomura, M., Auwerx, J., and Schoonjans, K. (2011) The bile acid membrane receptor TGR5 as an emerging target in metabolism and inflammation. J. Hepatol. 54, 1263-1272
20. Hov, J. R., Keitel, V., Laerdahl, J. K., Spomer, L., Ellinghaus, E., ElSharawy, A., Melum, E., Boberg, K. M., Manke, T., Balschun, T., Schramm, C., Bergquist, A., Weismüller, T., Gotthardt, D., Rust, C., Henckaerts, L., Onnie, C. M., Weersma, R. K., Sterneck, M., Teufel, A., Runz, H., Stiehl, A., Ponsioen, C. Y., Wijmenga, C., Vatn, M. H., IBSEN Study Group, Stokkers, P. C., Vermeire, S., Mathew, C. G., Lie, B. A., Beuers, U., Manns, M. P., Schreiber, S., Schrumpf, E., Häussinger, D., Franke, A., and Karlsen, T. H. (2010) Mutational characterization of the bile acid receptor TGR5 in primary sclerosing cholangitis. PLoS ONE 5, e12403
21. Rodriguez, M. C., Xie, Y. B., Wang, H., Collison, K., and Segaloff, D. L. (1992) Effects of truncations of the cytoplasmic tail of the luteinizing hormone/chorionic gonadotropin receptor on receptor-mediated hormone internalization. Mol. Endocrinol. 6, 327-336
22. Oksche, A., Dehe, M., Schülein, R., Wiesner, B., and Rosenthal, W. (1998) Folding and cell surface expression of the vasopressin V2 receptor. Requirement of the intracellular C terminus. FEBS Lett. 424, 57-62
23. Pankevych, H., Korkhov, V., Freissmuth, M., and Nanoff, C. (2003) Truncation of the A1 adenosine receptor reveals distinct roles of the membrane-proximal carboxyl terminus in receptor folding and G protein coupling. J. Biol. Chem. 278, 30283-30293
24. 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
25. Zhang, X., Dong, C., Wu, Q. J., Balch, W. E., and Wu, G. (2011) Di-Acidic motifs in the membrane-distal C termini modulate the transport of angiotensin II receptors from the endoplasmic reticulum to the cell surface. J. Biol. Chem. 286, 20525-20535
26. Duvernay, M. T., Zhou, F., and Wu, G. (2004) A conserved motif for the transport ofGprotein-coupled receptors from the endoplasmic reticulum to the cell surface. J. Biol. Chem. 279, 30741-30750
27. Ahn, K. H., Nishiyama, A., Mierke, D. F., and Kendall, D. A. (2010) Hydrophobic residues in helix 8 of cannabinoid receptor 1 are critical for structural and functional properties. Biochemistry 49, 502-511
28. Thielen, A., Oueslati, M., Hermosilla, R., Krause, G., Oksche, A., Rosenthal, W., and Schülein, R. (2005) The hydrophobic amino acid residues in the membrane-proximalCtail of theGprotein-coupled vasopressin V2 receptor are necessary for transport-competent receptor folding. FEBS Lett. 579, 5227-5235
29. Case, D. A., Cheatham, T. E., 3rd, Darden, T., Gohlke, H., Luo, R., Merz, K. M., Jr., Onufriev, A., Simmerling, C., Wang, B., and Woods, R. J. (2005) The Amber biomolecular simulation programs. J Comput. Chem. 26, 1668-1688
30. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117, 5179-5197
31. Simmerling, C., Strockbine, B., and Roitberg, A. E. (2002) All-Atom structure prediction and folding simulations of a stable protein. J. Am. Chem. Soc. 124, 11258-11259
32. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935
33. Darden, T., York, D., and Pedersen, L. (1993) Particle mesh Ewald. An N [center-dot] log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092
34. Ryckaert, J. P., Ciccotti, G., and Berendsen, H. J. C. (1977) Numerical integration of the cartesian equations of motion of a system with constraints. Molecular dynamics of n-Alkanes. J. Comput. Phys. 23, 327-341
35. Kabsch, W., and Sander, C. (1983) Dictionary of protein secondary structure. Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637
36. R-Development-Core-Team (2008) R, a language and environment for statistical computing. R-Foundation for Statistical Computing, Vienna, Austria
37. Sonnhammer, E. L., von Heijne, G., and Krogh, A. (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol. 6, 175-182
38. 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
39. Schülein, R., Hermosilla, R., Oksche, A., Dehe, M., Wiesner, B., Krause, G., and Rosenthal, W. (1998) A dileucine sequence and an upstream glutamate residue in the intracellular carboxyl terminus of the vasopressin V2 receptor are essential for cell surface transport in COS. M6 cells. Mol. Pharmacol. 54, 525-535
40. Chakrabartty, A., Schellman, J. A., and Baldwin, R. L. (1991) Large differences in the helix propensities of alanine and glycine. Nature 351, 586-588
41. Pace, C. N., and Scholtz, J. M. (1998) A helix propensity scale based on experimental studies of peptides and proteins. Biophys. J. 75, 422-427
42. Richardson, J. S. (1981) The anatomy and taxonomy of protein structure. Adv. Protein Chem. 34, 167-339
43. Cherezov, V., Rosenbaum, D. M., Hanson, M. A., Rasmussen, S. G., Thian, F. S., Kobilka, T. S., Choi, H. J., Kuhn, P., Weis, W. I., Kobilka, B. K., and Stevens, R. C. (2007) High-resolution crystal structure of an engineered human-2-Adrenergic G protein-coupled receptor. Science 318, 1258-1265
44. Rasmussen, S. G., Choi, H. J., Rosenbaum, D. M., Kobilka, T. S., Thian, F. S., Edwards, P. C., Burghammer, M., Ratnala, V. R., Sanishvili, R., Fischetti, R. F., Schertler, G. F., Weis, W. I., and Kobilka, B. K. (2007) Crystal structure of the human-2 adrenergic G-protein-coupled receptor. Nature 450, 383-387
45. Duvernay, M. T., Dong, C., Zhang, X., Zhou, F., Nichols, C. D., and Wu, G. (2009) Anterograde trafficking of G protein-coupled receptors. Function of the C-terminal FX6LL motif in export from the endoplasmic reticulum. Mol. Pharmacol. 75, 751-761
46. Hanson, M. A., Roth, C. B., Jo, E., Griffith, M. T., Scott, F. L., Reinhart, G., Desale, H., Clemons, B., Cahalan, S. M., Schuerer, S. C., Sanna, M. G., Han, G. W., Kuhn, P., Rosen, H., and Stevens, R. C. (2012) Crystal structure of a lipid G protein-coupled receptor. Science 335, 851-855
47. Wu, H., Wacker, D., Mileni, M., Katritch, V., Han, G. W., Vardy, E., Liu, W., Thompson, A. A., Huang, X. P., Carroll, F. I., Mascarella, S. W., Westkaemper, R. B., Mosier, P. D., Roth, B. L., Cherezov, V., and Stevens, R. C. (2012) Structure of the human-opioid receptor in complex with JDTic. Nature 485, 327-332
48. Lin, M. M., Mohammed, O. F., Jas, G. S., and Zewail, A. H. (2011) Speed limit of protein folding evidenced in secondary structure dynamics. Proc. Natl. Acad. Sci. U.S.A. 108, 16622-16627
49. Gnanakaran, S., Nymeyer, H., Portman, J., Sanbonmatsu, K. Y., and García, A. E. (2003) Peptide folding simulations. Curr. Opin. Struct. Biol. 13, 168-174
50. De Sancho, D., and Best, R. B. (2011) What Is the Time Scale for-helix nucleation? J. Am. Chem. Soc. 133, 6809-6816
51. Orel, M., Padrós, E., and Manyosa, J. (2012) Structural features of the C terminus from the human neurokinin-1 receptor. FEBS J. 279, 2357-2367
52. Wu, B., Chien, E. Y., Mol, C. D., Fenalti, G., Liu, W., Katritch, V., Abagyan, R., Brooun, A., Wells, P., Bi, F. C., Hamel, D. J., Kuhn, P., Handel, T. M., Cherezov, V., and Stevens, R. C. (2010) Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 330, 1066-1071
53. Hammad, M. M., Kuang, Y. Q., Morse, A., and Dupré, D. J. (2012) Rab1 interacts directly with the-2-Adrenergic receptor to regulate receptor anterograde trafficking. Biol. Chem. 393, 541-546
54. Golovin, A., and Henrick, K. (2008) MSDmotif. Exploring protein sites and motifs. BMC Bioinformatics 9, 312-319
55. Ahn, K. H., Pellegrini, M., Tsomaia, N., Yatawara, A. K., Kendall, D. A., and Mierke, D. F. (2009) Structural analysis of the human cannabinoid receptor one carboxyl-terminus identifies two amphipathic helices. Biopolymers 91, 565-573
56. Stadel, R., Ahn, K. H., and Kendall, D. A. (2011) The cannabinoid type-1 receptor carboxyl-terminus, more than just a tail. J Neurochem. 117, 1-18