Heterologous expression and purification of the serotonin type 4 receptor from transgenic mouse retina

Biochemistry

Volumn 47, Issue 50, 2008, Pages 13296-13307

  Salom, David ^a   Wu, Nan ^a   Sun, Wenyu ^a   Dong, Zhiqian ^a   Palczewski, Krzysztof ^b   Jordan, Steven ^c   Salon, John A ^c  

^a Polgenix Inc   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BIOCHEMISTRY; CELL MEMBRANES; CHROMATOGRAPHIC ANALYSIS; LIGANDS; OPHTHALMOLOGY; PROTEINS;

BINDING PROPERTIES; COUPLED RECEPTORS; DETERGENT SOLUTIONS; DRUG DESIGNS; EPITOPE SEQUENCES; EXPRESSION SYSTEMS; FUNCTIONAL CONFORMATIONS; FUSION PROTEINS; G PROTEINS; GLYCOSYLATED; HETEROLOGOUS EXPRESSIONS; IMMUNOAFFINITY CHROMATOGRAPHIES; IMMUNOBLOTTING; IN VITRO; IN-VIVO; INITIAL STATES; LIGAND BINDING PROPERTIES; MODIFIED PROTEINS; MOUSE OPSIN PROMOTERS; OUTER SEGMENTS; PHOTORECEPTOR SYSTEMS; PURIFIED RECEPTORS; RADIOLIGAND BINDINGS; RECEPTOR PROTEINS; TRANSGENIC MOUSE; X-RAY STRUCTURES;

PURIFICATION;

G PROTEIN COUPLED RECEPTOR; OPSIN; SEROTONIN 4 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IMMUNOAFFINITY CHROMATOGRAPHY; IMMUNOBLOTTING; LIGAND BINDING; MALE; MOUSE; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION; PROTEIN PURIFICATION; RADIOASSAY; RETINA; RETINA ROD OUTER SEGMENT; SOLUBILIZATION; TRANSGENIC MOUSE;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; FEMALE; GENE EXPRESSION REGULATION; GENE TARGETING; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; OPSINS; RECEPTORS, SEROTONIN, 5-HT4; RETINA; TRANSFECTION; XENOPUS LAEVIS;

MUS MUSCULUS;

EID: 57649118503     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi8018527     Document Type: Article

References (48)

1. Kroeze, W. K., Sheffler, D. J., and Roth, B. L. (2003) G-protein-coupled receptors at a glance. J. Cell Sci. 116, 4867-4869.
2. Armbruster, B. N., and Roth, B. L. (2005) Mining the receptorome. J. Biol. Chem. 280, 5129-5132.
3. Mustafi, D., and Palczewski, K. (2008) Topology of class A G protein-coupled receptors: Insights gained from crystal structures of rhodopsins, adrenergic and adenosine receptors. Mol. Pharmacol. (in press).
4. Okada, T., Takeda, K., and Kouyama, T. (1998) Highly selective separation of rhodopsin from bovine rod outer segment membranes using combination of divalent cation and alkyl(thio)glucoside. Photochem. Photobiol. 67, 495-499.
5. Okada, T., Le Trong, I., Fox, B. A., Behnke, C. A., Stenkamp, R. E., and Palczewski, K. (2000) X-ray diffraction analysis of three-dimensional crystals of bovine rhodopsin obtained from mixed micelles. J. Struct. Biol. 130, 73-80.
6. Teller, D. C., Okada, T., Behnke, C. A., Palczewski, K., and Stenkamp, R. E. (2001) Advances in determination of a high-resolution three-dimensional structure of rhodopsin, a model of G-protein-coupled receptors (GPCRs). Biochemistry 40, 7761-7772.
7. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le Trong, I., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M., and Miyano, M. (2000) Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289, 739-745.
8. Palczewski, K. (2006) G protein-coupled receptor rhodopsin. Annu. Rev. Biochem. 75, 743-767.
9. Zhang, L., Salom, D., He, J., Okun, A., Ballesteros, J., Palczewski, K., and Li, N. (2005) Expression of Functional G Protein-Coupled Receptors in Photoreceptors of Transgenic Xenopus laevis. Biochemistry 44, 14509-14518.
10. Panneels, V., Eroglu, C., Cronet, P., and Sinning, I. (2003) Pharmacological characterization and immunoaffinity purification of metabotropic glutamate receptor from Drosophila overexpressed in Sf9 cells. Protein Expression Purif. 30, 275-282.
11. Eroglu, C., Cronet, P., Panneels, V., Beaufils, P., and Sinning, I. (2002) Functional reconstitution of purified metabotropic glutamate receptor expressed in the fly eye. EMBO Rep. 3, 491-496.
12. Li, N., Salom, D., Zhang, L., Harris, T., Ballesteros, J. A., Golczak, M., Jastrzebska, B., Palczewski, K., Kurahara, C., Juan, T., Jordan, S., and Salon, J. A. (2007) Heterologous expression of the adenosine A1 receptor in transgenic mouse retina. Biochemistry 46, 8350-8359.
13. Lem, J., Applebury, M. L., Falk, J. D., Flannery, J. G., and Simon, M. I. (1991) Tissue-specific and developmental regulation of rod opsin chimeric genes in transgenic mice. Neuron 6, 201-210.
14. Zack, D. J., Bennett, J., Wang, Y., Davenport, C., Klaunberg, B., Gearhart, J., and Nathans, J. (1991) Unusual topography of bovine rhodopsin promoter-lacZ fusion gene expression in transgenic mouse retinas. Neuron 6, 187-199.
15. al-Ubaidi, M. R., Pittler, S. J., Champagne, M. S., Triantafyllos, J. T., McGinnis, J. F., and Baehr, W. (1990) Mouse opsin. Gene structure and molecular basis of multiple transcripts. J. Biol. Chem. 265, 20563-20569.
16. MacKenzie, D., Arendt, A., Hargrave, P., McDowell, J. H., and Molday, R. S. (1984) Localization of binding sites for carboxyl terminal specific anti-rhodopsin monoclonal antibodies using synthetic peptides. Biochemistry 23, 6544-6549.
17. Kashanchi, F., Thompson, J., Sadaie, M. R., Doniger, J., Duvall, J., Brady, J. N., and Rosenthal, L. J. (1994) Transcriptional activation of minimal HIV-1 promoter by ORF-1 protein expressed from the SalI-L fragment of human herpesvirus 6. Virology 201, 95-106.
18. Batten, M. L., Imanishi, Y., Maeda, T., Tu, D. C., Moise, A. R., Bronson, D., Possin, D., Van Gelder, R. N., Baehr, W., and Palczewski, K. (2004) Lecithin-retinol acyltransferase is essential for accumulation of all-trans-retinyl esters in the eye and in the liver. J. Biol. Chem. 279, 10422-10432.
19. Maeda, A., Maeda, T., Imanishi, Y., Kuksa, V., Alekseev, A., Bronson, J. D., Zhang, H., Zhu, L., Sun, W., Saperstein, D. A., Rieke, F., Baehr, W., and Palczewski, K. (2005) Role of photoreceptor-specific retinol dehydrogenase in the retinoid cycle in vivo. J. Biol. Chem. 280, 18822-18832.
20. Imanishi, Y., Batten, M. L., Piston, D. W., Baehr, W., and Palczewski, K. (2004) Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye. J. Cell Biol. 164, 373-383.
21. Adamus, G., Zam, Z. S., Arendt, A., Palczewski, K., McDowell, J. H., and Hargrave, P. A. (1991) Anti-rhodopsin monoclonal antibodies of defined specificity: Characterization and application. Vision Res. 31, 17-31.
22. Cheng, Y., and Prusoff, W. H. (1973) Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50% inhibition (150) of an enzymatic reaction. Biochem. Pharmacol. 22, 3099-3108.
23. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
24. Salom, D., Lodowski, D. T., Stenkamp, R. E., Le Trong, I., Golczak, M., Jastrzebska, B., Harris, T., Ballesteros, J. A., and Palczewski, K. (2006) Crystal structure of a photoactivated deprotonated intermediate of rhodopsin. Proc. Natl. Acad. Sci. U.S.A. 103, 16123-16128.
25. Chen, J., Makino, C. L., Peachey, N. S., Baylor, D. A., and Simon, M. I. (1995) Mechanisms of rhodopsin inactivation in vivo as revealed by a COOH-terminal truncation mutant. Science 267, 374-377.
26. Breathnach, R., and Harris, B. A. (1983) Plasmids for the cloning and expression of full-length double-stranded cDNAs under control of the SV40 early or late gene promoter. Nucleic Acids Res. 11, 7119-7136.
27. Palczewski, K., Farber, D. B., and Hargrave, P. A. (1991) Elevated level of protein phosphatase 2A activity in retinas of rd mice. Exp. Eye Res. 53, 101-105.
28. Labrecque, J., Fargin, A., Bouvier, M., Chidiac, P., and Dennis, M. (1995) Serotonergic antagonists differentially inhibit spontaneous activity and decrease ligand binding capacity of the rat 5-hydroxytryptamine type 2C receptor in Sf9 cells. Mol. Pharmacol. 48, 150-159.
29. Eglen, R. M., Wong, E. H., Dumuis, A., and Bockaert, J. (1995) Central 5-HT4 receptors. Trends Pharmacol. Sci. 16, 391-398.
30. McLean, P. G., and Coupar, I. M. (1995) 5-HT4 receptor antagonist affinities of SB207710, SB205008, and SB203186 in the human colon, rat oesophagus, and guinea-pig ileum peristaltic reflex. Naunyn-Schmiedeberg's Arch. Pharmacol. 352, 132-140.
31. Van den Wyngaert, I., Gommeren, W., Verhasselt, P., Jurzak, M., Leysen, J., Luyten, W., and Bender, E. (1997) Cloning and expression of a human serotonin 5-HT4 receptor cDNA. J. Neurochem. 69, 1810-1819.
32. Park, P. S., Sum, C. S., Pawagi, A. B., and Wells, J. W. (2002) Cooperativity and oligomeric status of cardiac muscarinic cholinergic receptors. Biochemistry 41, 5588-5604.
33. Lundstrom, K. (2005) The future of G protein-coupled receptors as targets in drug discovery. IDrugs 8, 909-913.
34. Geertsma, E. R., Nik Mahmood, N. A., Schuurman-Wolters, G. K., and Poolman, B. (2008) Membrane reconstitution of ABC transporters and assays of translocator function. Nat. Protoc. 3, 256-266.
35. Geertsma, E. R., Groeneveld, M., Slotboom, D. J., and Poolman, B. (2008) Quality control of overexpressed membrane proteins. Proc. Natl. Acad. Sci. U.S.A. 105, 5722-5727.
36. 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 β2-adrenergic G protein-coupled receptor. Science 318, 1258-1265.
37. McCusker, E. C., Bane, S. E., O'Malley, M. A., and Robinson, A. S. (2007) Heterologous GPCR expression: A bottleneck to obtaining crystal structures. Biotechnol. Prog. 23, 540-547.
38. Serrano-Vega, M. J., Magnani, F., Shibata, Y., and Tate, C. G. (2008) Conformational thermostabilization of the β1-adrenergic receptor in a detergent-resistant form. Proc. Natl. Acad. Sci. U.S.A. 105, 877-882.
39. Klammt, C., Schwarz, D., Eifler, N., Engel, A., Piehler, J., Haase, W., Hahn, S., Dotsch, V., and Bernhard, F. (2007) Cell-free production of G protein-coupled receptors for functional and structural studies. J. Struct. Biol. 158, 482-493.
40. Markkanen, P. M., and Petaja-Repo, U. E. (2008) N-Glycan-mediated Quality Control in the Endoplasmic Reticulum Is Required for the Expression of Correctly Folded δ-Opioid Receptors at the Cell Surface. J. Biol. Chem. 283, 29086-29098.
41. Kaushal, S., Ridge, K. D., and Khorana, H. G. (1994) Structure and function in rhodopsin: The role of asparagine-linked glycosylation. Proc. Natl. Acad. Sci. U.S.A. 91, 4024-4028.
42. Sung, C. H., Schneider, B. G., Agarwal, N., Papermaster, D. S., and Nathans, J. (1991) Functional heterogeneity of mutant rhodopsins responsible for autosomal dominant retinitis pigmentosa. Proc. Natl. Acad. Sci. U.S.A. 88, 8840-8844.
43. Morello, J. P., Salahpour, A., Laperriere, A., Bernier, V., Arthus, M. F., Lonergan, M., Petaja-Repo, U., Angers, S., Morin, D., Bichet, D. G., and Bouvier, M. (2000) Pharmacological chaperones rescue cell-surface expression and function of misfolded V2 vasopressin receptor mutants. J. Clin. Invest. 105, 887-895.
44. Morello, J. P., Petaja-Repo, U. E., Bichet, D. G., and Bouvier, M. (2000) Pharmacological chaperones: A new twist on receptor folding. Trends Pharmacol. Sci. 21, 466-469.
45. +)-ATPase from rectal glands of Squalus acanthias. Biochim. Biophys. Acta 567, 410-420.
46. +)-ATPase. Biochim. Biophys. Acta 787, 81-89.
47. Breyton, C., Tribet, C., Olive, J., Dubacq, J. P., and Popot, J. L. (1997) Dimer to monomer conversion of the cytochrome b6f complex. Causes and consequences. J. Biol. Chem. 272, 21892-21900.
48. Sarramegna, V., Muller, I., Milon, A., and Talmont, F. (2006) Recombinant G protein-coupled receptors from expression to renaturation: A challenge towards structure. Cell. Mol. Life Sci. 63, 1149-1164.