The oligomeric states of the purified sigma-1 receptor are stabilized by ligands

Journal of Biological Chemistry

Volumn 289, Issue 29, 2014, Pages 20333-20344

  Gromek, Katarzyna A ^a   Suchy, Fabian P ^a   Meddaugh, Hannah R ^a   Wrobel, Russell L ^a   LaPointe, Loren M ^a   Chu, Uyen B ^b   Primm, John G ^a   Ruoho, Arnold E ^b   Senes, Alessandro ^a   Fox, Brian G ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; MAMMALS; MOLECULES; OLIGOMERS; PROTEINS; SPHINGOSINES;

AMYOTROPHIC LATERAL SCLEROSIS; ELEVATED TEMPERATURE; LIGAND BINDING ACTIVITY; MEMBRANE PROTEINS; MOLECULAR REGULATION; NEUROLOGICAL DISORDERS; POSSIBLE MECHANISMS; TRANSMEMBRANE REGIONS;

LIGANDS;

HALOPERIDOL; MONOMER; N [2 (3,4 DICHLOROPHENYL)ETHYL] 2 DIMETHYLAMINO N METHYLETHYLAMINE; OLIGOMER; PENTAZOCINE; SIGMA 1 OPIATE RECEPTOR; SPHINGOSINE; TRITIUM;

ARTICLE; BINDING ASSAY; CONTROLLED STUDY; DIMERIZATION; GEL FILTRATION CHROMATOGRAPHY; GEL PERMEATION CHROMATOGRAPHY; HIGH TEMPERATURE; IN VITRO STUDY; LIGAND BINDING; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN PURIFICATION; PROTEIN STABILITY; TEMPERATURE SENSITIVITY;

GXXXG MOTIF; LIGAND-BINDING PROTEIN; MEMBRANE PROTEIN; PROTEIN-PROTEIN INTERACTION; SIGNAL TRANSDUCTION; Σ RECEPTOR;

AMINO ACID MOTIFS; AMINO ACID SUBSTITUTION; ANIMALS; CROSS-LINKING REAGENTS; GUINEA PIGS; HALOPERIDOL; HUMANS; LIGANDS; MALTOSE-BINDING PROTEINS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PENTAZOCINE; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; RECEPTORS, SIGMA; RECOMBINANT FUSION PROTEINS;

EID: 84904497999     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.537993     Document Type: Article

References (74)

1. Hanner, M., Moebius, F. F., Flandorfer, A., Knaus, H. G., Striessnig, J., Kempner, E., and Glossmann, H. (1996) Purification, molecular cloning, and expression of the mammalian sigma1-binding site. Proc. Natl. Acad. Sci. U.S.A. 93, 8072-8077 (Pubitemid 26277167)
2. Jbilo, O., Vidal, H., Paul, R., De Nys, N., Bensaid, M., Silve, S., Carayon, P., Davi, D., Galiègue, S., Bourrié, B., Guillemot, J. C., Ferrara, P., Loison, G., Maffrand, J. P., Le Fur, G., and Casellas, P. (1997) Purification and characterization of the human SR 31747A-binding protein. A nuclear membrane protein related to yeast sterol isomerase. J. Biol. Chem. 272, 27107-27115 (Pubitemid 27452667)
3. Kekuda, R., Prasad, P. D., Fei, Y. J., Leibach, F. H., and Ganapathy, V. (1996) Cloning and functional expression of the human type 1 sigma receptor (hSigmaR1). Biochem. Biophys. Res. Commun. 229, 553-558 (Pubitemid 27029069)
4. Seth, P., Leibach, F. H., and Ganapathy, V. (1997) Cloning and structural analysis of the cDNA and the gene encoding the murine type 1 sigma receptor. Biochem. Biophys. Res. Commun. 241, 535-540 (Pubitemid 28020136)
5. Su, T. P., Hayashi, T., Maurice, T., Buch, S., and Ruoho, A. E. (2010) The sigma-1 receptor chaperone as an inter-organelle signaling modulator. Trends Pharmacol. Sci. 31, 557-566
6. Ha, Y., Dun, Y., Thangaraju, M., Duplantier, J., Dong, Z., Liu, K., Ganapathy, V., and Smith, S. B. (2011) Sigma receptor 1 modulates endoplasmic reticulum stress in retinal neurons. Invest. Ophthalmol. Vis. Sci. 52, 527-540
7. Hayashi, T., and Fujimoto, M. (2010) Detergent-resistant microdomains determine the localization of sigma-1 receptors to the endoplasmic reticulum-mitochondria junction. Mol. Pharmacol. 77, 517-528
8. Hayashi, T., Justinova, Z., Hayashi, E., Cormaci, G., Mori, T., Tsai, S. Y., Barnes, C., Goldberg, S. R., and Su, T. P. (2010) Regulation of sigma-1 receptors and endoplasmic reticulum chaperones in the brain of methamphetamine self-administering rats. J. Pharmacol. Exp. Ther. 332, 1054-1063
9. Aydar, E., Palmer, C. P., Klyachko, V. A., and Jackson, M. B. (2002) The sigma receptor as a ligand-regulated auxiliary potassium channel subunit. Neuron 34, 399-410 (Pubitemid 34465498)
10. Mavlyutov, T. A., Epstein, M. L., Andersen, K. A., Ziskind-Conhaim, L., and Ruoho, A. E. (2010) The sigma-1 receptor is enriched in postsynaptic sites of C termini in mouse motoneurons. An anatomical and behavioral study. Neuroscience 167, 247-255
11. Mavlyutov, T. A., Epstein, M. L., Liu, P., Verbny, Y. I., Ziskind-Conhaim, L., and Ruoho, A. E. (2012) Development of the sigma-1 receptor in C termini of motoneurons and colocalization with the N,N′- dimethyltryptamine forming enzyme, indole-N-methyl transferase. Neuroscience 206, 60-68
12. Gundlach, A. L., Largent, B. L., and Snyder, S. H. (1986) Autoradiographic localization of sigma receptor binding sites in guinea pig and rat central nervous system with (+)3H-3-(3-hydroxyphenyl)-N-(1-propyl) piperidine. J. Neurosci. 6, 1757-1770 (Pubitemid 16078351)
13. Moebius, F. F., Bermoser, K., Reiter, R. J., Hanner, M., and Glossmann, H. (1996) Yeast sterol C8-C7 isomerase: identification and characterization of a high-affinity binding site for enzyme inhibitors. Biochemistry 35, 16871-16878 (Pubitemid 27020533)
14. Hayashi, T., and Su, T. P. (2001) Regulating ankyrin dynamics: roles of sigma-1 receptors. Proc. Natl. Acad. Sci. U.S.A. 98, 491-496 (Pubitemid 32105069)
15. 2+ signaling and cell survival. Cell 131, 596-610
16. Navarro, G., Moreno, E., Aymerich, M., Marcellino, D., McCormick, P. J., Mallol, J., Cortés, A., Casadó, V., Canela, E. I., Ortiz, J., Fuxe, K., Lluís, C., Ferré, S., and Franco, R. (2010) Direct involvement of sigma-1 receptors in the dopamine D1 receptor-mediated effects of cocaine. Proc. Natl. Acad. Sci. U.S.A. 107, 18676-18681
17. Kim, F. J., Kovalyshyn, I., Burgman, M., Neilan, C., Chien, C. C., and Pasternak, G. W. (2010) Sigma 1 receptor modulation of G-protein-coupled receptor signaling: potentiation of opioid transduction independent from receptor binding. Mol. Pharmacol. 77, 695-703
18. Villard, V., Espallergues, J., Keller, E., Vamvakides, A., and Maurice, T. (2011) Anti-amnesic and neuroprotective potentials of the mixed muscarinic receptor/sigma-1 (sigma1) ligand ANAVEX2-73, a novel aminotetrahydrofuran derivative. J. Psychopharmacol. 25, 1101-1117
19. + channel modulation in rodent neurohypophysial nerve terminals by sigma receptors and not by dopamine receptors. J. Physiol. 517, 391-406
20. Johannessen, M., Ramachandran, S., Riemer, L., Ramos-Serrano, A., Ruoho, A. E., and Jackson, M. B. (2009) Voltage-gated sodium channel modulation by sigma-receptors in cardiac myocytes and heterologous systems. Am. J. Physiol. Cell Physiol 296, C1049-C1057
21. Zhang, M. R., Haradahira, T., Maeda, J., Okauchi, T., Kawabe, K., Kida, T., Obayashi, S., Suzuki, K., and Suhara, T. (2002) Synthesis and evaluation of 3-(4-chlorobenzyl)-8-[11C]methoxy-1,2,3,4-tetrahydrochromeno[3,4-c] pyridin-5-one: a PET tracer for imaging sigma(1) receptors. Nucl. Med. Biol. 29, 469-476 (Pubitemid 34597119)
22. + channels in rat neurohypophysial terminals requires neither G-protein nor ATP. J. Physiol. 526, 527-539
23. Carnally, S. M., Johannessen, M., Henderson, R. M., Jackson, M. B., and Edwardson, J. M. (2010) Demonstration of a direct interaction between sigma-1 receptors and acid-sensing ion channels. Biophys. J. 98, 1182-1191
24. Bucolo, C., Drago, F., Lin, L. R., and Reddy, V. N. (2006) Sigma receptor ligands protect human retinal cells against oxidative stress. Neuroreport 17, 287-291
25. Wang, L., Eldred, J. A., Sidaway, P., Sanderson, J., Smith, A. J., Bowater, R. P., Reddan, J. R., and Wormstone, I. M. (2012) Sigma 1 receptor stimulation protects against oxidative damage through suppression of the ER stress responses in the human lens. Mech. Ageing Dev. 133, 665-674
26. Pal, A., Fontanilla, D., Gopalakrishnan, A., Chae, Y. K., Markley, J. L., and Ruoho, A. E. (2012) The sigma-1 receptor protects against cellular oxidative stress and activates antioxidant response elements. Eur. J. Pharmacol. 682, 12-20
27. 3H]3-PPP. Eur. J. Pharmacol. 124, 183-187
28. 3H]SKF 10047 binding sites in rat brain membranes: evidence of multiplicity. Eur. J. Pharmacol. 136, 231-234
29. Martin, W. R., Eades, C. G., Thompson, J. A., Huppler, R. E., and Gilbert, P. E. (1976) The effects of morphine-and nalorphine-like drugs in the nondependent and morphine-dependent chronic spinal dog. J. Pharmacol. Exp. Ther. 197, 517-532
30. Fontanilla, D., Johannessen, M., Hajipour, A. R., Cozzi, N. V., Jackson, M. B., and Ruoho, A. E. (2009) The hallucinogen N,N-dimethyltryptamine (DMT) is an endogenous sigma-1 receptor regulator. Science 323, 34-937
31. Ramachandran, S., Chu, U. B., Mavlyutov, T. A., Pal, A., Pyne, S., and Ruoho, A. E. (2009) The sigma1 receptor interacts with N-alkyl amines and endogenous sphingolipids. Eur. J. Pharmacol. 609, 19-26
32. Su, T. P., London, E. D., and Jaffe, J. H. (1988) Steroid binding at sigma receptors suggests a link between endocrine, nervous, and immune systems. Science 240, 219-221
33. Moriguchi, S., Yamamoto, Y., Ikuno, T., and Fukunaga, K. (2011) Sigma-1 receptor stimulation by dehydroepiandrosterone ameliorates cognitive impairment through activation of CaM kinase II, protein kinase C and extracellular signal-regulated kinase in olfactory bulbectomized mice. J. Neurochem. 117, 879-891
34. Cobos, E. J., Entrena, J. M., Nieto, F. R., Cendán, C. M., and Del Pozo, E. (2008) Pharmacology and therapeutic potential of sigma(1) receptor ligands. Curr. Neuropharmacol. 6, 344-366
35. Al-Saif, A., Al-Mohanna, F., and Bohlega, S. (2011) A mutation in sigma-1 receptor causes juvenile amyotrophic lateral sclerosis. Ann. Neurol. 70, 913-919
36. Mishina, M., Ohyama, M., Ishii, K., Kitamura, S., Kimura, Y., Oda, K., Kawamura, K., Sasaki, T., Kobayashi, S., Katayama, Y., and Ishiwata, K. (2008) Low density of sigma1 receptors in early Alzheimer's disease. Ann. Nucl. Med. 22, 151-156 (Pubitemid 351729624)
37. Mishina, M., Ishiwata, K., Ishii, K., Kitamura, S., Kimura, Y., Kawamura, K., Oda, K., Sasaki, T., Sakayori, O., Hamamoto, M., Kobayashi, S., and Katayama, Y. (2005) Function of sigma1 receptors in Parkinson's disease. Acta Neurol. Scand. 112, 103-107 (Pubitemid 41003370)
38. Smith, S. B., Duplantier, J., Dun, Y., Mysona, B., Roon, P., Martin, P. M., and Ganapathy, V. (2008) In vivo protection against retinal neurodegeneration by sigma receptor 1 ligand (+)-pentazocine. Invest. Ophthalmol. Vis. Sci. 49, 4154-4161
39. Hiranita, T., Soto, P. L., Tanda, G., and Katz, J. L. (2010) Reinforcing effects of sigma-receptor agonists in rats trained to self-administer cocaine. J. Pharmacol. Exp. Ther. 332, 515-524
40. Ujike, H., Kuroda, S., and Otsuki, S. (1996) Sigma receptor antagonists block the development of sensitization to cocaine. Eur. J. Pharmacol. 296, 123-128
41. Ramachandran, S., Lu, H., Prabhu, U., and Ruoho, A. E. (2007) Purification and characterization of the guinea pig sigma-1 receptor functionally expressed in Escherichia coli. Protein Expr. Purif. 51, 283-292 (Pubitemid 44821877)
42. Chen, Y., Hajipour, A. R., Sievert, M. K., Arbabian, M., and Ruoho, A. E. (2007) Characterization of the cocaine binding site on the sigma-1 receptor. Biochemistry 46, 3532-3542 (Pubitemid 46449170)
43. Fontanilla, D., Hajipour, A. R., Pal, A., Chu, U. B., Arbabian, M., and Ruoho, A. E. (2008) Probing the steroid binding domain-like I (SBDLI) of the sigma-1 receptor binding site using N-substituted photoaffinity labels. Biochemistry 47, 7205-7217 (Pubitemid 351956369)
44. Pal, A., Hajipour, A. R., Fontanilla, D., Ramachandran, S., Chu, U. B., Mavlyutov, T., and Ruoho, A. E. (2007) Identification of regions of the sigma-1 receptor ligand binding site using a novel photoprobe. Mol. Pharmacol. 72, 921-933 (Pubitemid 47481415)
45. Pal, A., Chu, U. B., Ramachandran, S., Grawoig, D., Guo, L. W., Hajipour, A. R., and Ruoho, A. E. (2008) Juxtaposition of the steroid binding domain-like I and II regions constitutes a ligand binding site in the sigma-1 receptor. J. Biol. Chem. 283, 19646-19656
46. Ganapathy, M. E., Prasad, P. D., Huang, W., Seth, P., Leibach, F. H., and Ganapathy, V. (1999) Molecular and ligand-binding characterization of the sigma-receptor in the Jurkat human T lymphocyte cell line. J. Pharmacol. Exp. Ther. 289, 251-260 (Pubitemid 29156037)
47. Seth, P., Ganapathy, M. E., Conway, S. J., Bridges, C. D., Smith, S. B., Casellas, P., and Ganapathy, V. (2001) Expression pattern of the type 1 sigma receptor in the brain and identity of critical anionic amino acid residues in the ligand-binding domain of the receptor. Biochim Biophys. Acta 1540, 59-67 (Pubitemid 32710049)
48. Russ, W. P., and Engelman, D. M. (2000) The GxxxG motif: a framework for transmembrane helix-helix association. J. Mol. Biol. 296, 911-919
49. Senes, A., Engel, D. E., and DeGrado, W. F. (2004) Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr. Opin. Struct. Biol. 14, 465-479 (Pubitemid 39094354)
50. Senes, A., Gerstein, M., and Engelman, D. M. (2000) Statistical analysis of amino acid patterns in transmembrane helices: the GxxxG motif occurs frequently and in association with β-branched residues at neighboring positions. J. Mol. Biol. 296, 921-936
51. Klock, H. E., and Lesley, S. A. (2009) The polymerase incomplete primer extension (PIPE) method applied to high-throughput cloning and site-directed mutagenesis. Methods Mol. Biol. 498, 91-103
52. Gromek, K. A., Meddaugh, H. R., Wrobel, R. L., Suchy, F. P., Bingman, C. A., Primm, J. G., and Fox, B. G. (2013) Improved expression and purification of sigma-1 receptor fused to maltose binding protein by alteration of linker sequence. Protein Expr. Purif. 89, 203-209
53. Russ, W. P., and Engelman, D. M. (1999) TOXCAT: a measure of transmembrane helix association in a biological membrane. Proc. Natl. Acad. Sci. U.S.A. 96, 863-868 (Pubitemid 29072149)
54. Blommel, P. G., and Fox, B. G. (2007) A combined approach to improving large-scale production of tobacco etch virus protease. Protein Expr. Purif. 55, 53-68 (Pubitemid 47259692)
55. Shaw, W. V. (1975) Chloramphenicol acetyltransferase from chloram-phenicol-resistant bacteria. Methods Enzymol. 43, 737-755
56. Narayanan, S., Bhat, R., Mesangeau, C., Poupaert, J. H., and McCurdy, C. R. (2011) Early development of sigma-receptor ligands. Future Med. Chem. 3, 79-94
57. Su, T. P., and Hayashi, T. (2003) Understanding the molecular mechanism of sigma-1 receptors: toward a hypothesis that sigma-1 receptors are intracellular amplifiers for signal transduction. Curr. Med. Chem. 10, 2073-2080
58. Matsumoto, R. R., Bowen, W. D., Tom, M. A., Vo, V. N., Truong, D. D., and De Costa, B. R. (1995) Characterization of two novel sigma receptor ligands: antidystonic effects in rats suggests s receptor antagonism. Eur. J. Pharmacol. 280, 301-310
59. Herrmann, J. R., Panitz, J. C., Unterreitmeier, S., Fuchs, A., Frishman, D., and Langosch, D. (2009) Complex patterns of histidine, hydroxylated amino acids and the GxxxG motif mediate high-affinity transmembrane domain interactions. J. Mol. Biol. 385, 912-923
60. Colabufo, N. A., Contino, M., Inglese, C., Niso, M., Perrone, R., Roperto, S., and Roperto, F. (2009) In vitro and ex vivo characterization of sigma-1 and sigma-2 receptors: agonists and antagonists in biological assays. Cent. Nerv. Syst. Agents Med. Chem. 9, 161-171
61. Yamamoto, H., Miura, R., Yamamoto, T., Shinohara, K., Watanabe, M., Okuyama, S., Nakazato, A., and Nukada, T. (1999) Amino acid residues in the transmembrane domain of the type 1 sigma receptor critical for ligand binding. FEBS Lett. 445, 19-22 (Pubitemid 29101527)
62. Wu, Z., and Bowen, W. D. (2008) Role of sigma-1 receptor C-terminal segment in inositol 1,4,5-trisphosphate receptor activation: constitutive enhancement of calcium signaling in MCF-7 tumor cells. J. Biol. Chem. 283, 28198-28215
63. Ortega-Roldan, J. L., Ossa, F., and Schnell, J. R. (2013) Characterization of the human sigma-1 receptor chaperone domain structure and binding immunoglobulin protein (BiP) interactions. J. Biol. Chem. 288, 21448-21457
64. Chu, U. B., Ramachandran, S., Hajipour, A. R., and Ruoho, A. E. (2013) Photoaffinity labeling of the sigma-1 receptor with N-[3-(4-Nitrophenyl)propyl]- N-dodecylamine: evidence of receptor dimers. Biochemistry 52, 859-868
65. Schuster, D. I., Arnold, F. J., and Murphy, R. B. (1995) Purification, pharmacological characterization and photoaffinity labeling of sigma receptors from rat and bovine brain. Brain Res. 670, 14-28
66. Casadó, V., Cortés, A., Mallol, J., Pérez-Capote, K., Ferré, S., Lluis, C., Franco, R., and Canela, E. I. (2009) GPCR homomers and heteromers: a better choice as targets for drug development than GPCR monomers? Pharmacol. Ther. 124, 248-257
67. Ferré, S., and Franco, R. (2010) Oligomerization of G-protein-coupled receptors: a reality. Curr. Opin. Pharmacol. 10, 1-5
68. Rovira, X., Pin, J. P., and Giraldo, J. (2010) The asymmetric/symmetric activation of GPCR dimers as a possible mechanistic rationale for multiple signalling pathways. Trends Pharmacol. Sci. 31, 15-21
69. Löw, C., Moberg, P., Quistgaard, E. M., Hedrén, M., Guettou, F., Frauenfeld, J., Haneskog, L., and Nordlund, P. (2013) High-throughput analytical gel filtration screening of integral membrane proteins for structural studies. Biochim Biophys. Acta 1830, 3497-3508
70. Na, J. H., Shin, J., Jung, Y., Lim, D., Shin, Y. K., and Yu, Y. G. (2013) Bacterially expressed human serotonin receptor 3A is functionally reconstituted in proteoliposomes. Protein Expr. Purif. 88, 190-195
71. Venkatakrishnan, A. J., Deupi, X., Lebon, G., Tate, C. G., Schertler, G. F., and Babu, M. M. (2013) Molecular signatures of G-protein-coupled receptors. Nature 494, 185-194
72. Vukoti, K., Kimura, T., Macke, L., Gawrisch, K., and Yeliseev, A. (2012) Stabilization of functional recombinant cannabinoid receptor CB(2) in detergent micelles and lipid bilayers. PLoS One 7, e46290
73. + channel with 4-fold symmetry. J. Biol. Chem. 287, 37021-37029
74. Brune, S., Schepmann, D., Lehmkuhl, K., Frehland, B., and Wünsch, B. (2012) Characterization of ligand binding to the sigma(1) receptor in a human tumor cell line (RPMI 8226) and establishment of a competitive receptor binding assay. Assay Drug Dev. Technol. 10, 365-374