A direct interaction between the sigma-1 receptor and the herg voltage-gated K+ channel revealed by atomic force microscopy and homogeneous time-resolved fluorescence (HTRF®)

Journal of Biological Chemistry

Volumn 289, Issue 46, 2014, Pages 32353-32363

  Balasuriya, Dilshan ^a   D'Sa, Lauren ^a   Talker, Ronel ^a   Dupuis, Elodie ^b   Maurin, Fabrice ^b   Martin, Patrick ^c   Borgese, Franck ^c   Soriani, Olivier ^c   Edwardson, J Michael ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b CisBio Bioassays Parc Marcel Boiteux ^*  (France)

^c CENTRE DE BIOCHIMIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMIC FORCE MICROSCOPY; DIMERS; FLUORESCENCE; MONOMERS; OLIGOMERS; PROTEINS;

CHOLESTEROL DEPLETION; DIRECT BINDINGS; DIRECT INTERACTIONS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM CHAPERONE; HEK293 CELLS; PERIPHERAL TISSUE; TIME-RESOLVED FLUORESCENCE;

CELL MEMBRANES;

POTASSIUM CHANNEL HERG; SIGMA 1 OPIATE RECEPTOR; CHOLESTEROL; COMPLEMENTARY DNA; EPITOPE; ERG1 POTASSIUM CHANNEL; ION; LIGAND; SIGMA OPIATE RECEPTOR; SIGMA-1 RECEPTOR;

ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING SITE; CELL MEMBRANE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FLUORESCENCE IMAGING; HOMOGENEOUS TIME RESOLVED FLUORESCENCE; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; CELL MOTION; FLUORESCENCE MICROSCOPY; GENETIC TRANSFECTION; HEK293 CELL LINE; HUMAN; METABOLISM;

CELL MEMBRANE; CELL MOVEMENT; CHOLESTEROL; DNA, COMPLEMENTARY; ENDOPLASMIC RETICULUM; EPITOPES; ETHER-A-GO-GO POTASSIUM CHANNELS; HEK293 CELLS; HUMANS; IONS; LIGANDS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, FLUORESCENCE; RECEPTORS, SIGMA; TRANSFECTION;

EID: 84910643248     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.603506     Document Type: Article

References (65)

1. 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
2. 2+: clinical and therapeutic relevance. Biol. Cell 97, 873-883
3. Tsai, S. Y., Hayashi, T., Mori, T., and Su, T.-P. (2009) Sigma-1 receptor chaperones and diseases. Cent. Nerv. Syst. Agents Med. Chem. 9, 184-189
4. 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
5. Tsai, S. Y., Hayashi, T., Harvey, B. K., Wang, Y., Wu, W. W., Shen, R. F., Zhang, Y., Becker, K. G., Hoffer, B. J., and Su, T.-P. (2009) Sigma-1 receptors regulate hippocampal dendritic spine formation via a free radicalsensitive mechanism involving Rac1•GTP pathway. Proc. Natl. Acad. Sci. U.S.A. 106, 22468-22473
6. 2+ signalling and cell survival. Cell 131, 596-610
7. Lysko, P. G., Gagnon, R. C., Yue, T. L., Gu, J. L., and Feuerstein, G. (1992) Neuroprotective effects of SKF 10,047 in cultured rat cerebellar neurons and in gerbil global brain ischemia. Stroke 23, 414-419
8. Ishiguro, H., Ohtsuki, T., Toru, M., Itokawa, M., Aoki, J., Shibuya, H., Kurumaji, A., Okubo, Y., Iwawaki, A., Ota, K., Shimizu, H., Hamaguchi, H., and Arinami, T. (1998) Association between polymorphisms in the type 1 σ receptor gene and schizophrenia. Neurosci. Lett. 257, 45-48
9. 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 sigma-1 receptors in early Alzheimer's disease. Ann. Nucl. Med. 22, 151-156
10. Fishback, J. A., Robson, M. J., Xu, Y. T., and Matsumoto, R. R. (2010) Sigma receptors: potential targets for a new class of antidepressant drugs. Pharmacol. Ther. 127, 271-282
11. 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
12. Aydar, E., Onganer, P., Perrett R., Djamgoz, M. B., and Palmer, C. P. (2006) The expression and functional characterization of sigma 1 receptors in breast cancer cell lines. Cancer Lett. 242, 245-257
13. Wang, B., Rouzier, R., Albarradn, C. T., Sahin, A., Wagner, P., Yang, Y., Smith, T. L., Meric-Bernstam, F., Marcelo Aldaz, C., Hortobagyi, G. N., and Pusztai, L. (2004) Expression of sigma-1 receptor in human breast cancer. Breast Cancer Res. Treat. 87, 205-214
14. - channels. J. Biol. Chem. 282, 2259-2267
15. kip1 accumulation. J. Pharmacol. Exp. Ther. 311, 1105-1114
16. Spruce, B. A., Campbell, L. A., McTavish, N., Cooper, M. A., Appleyard, M. V., O'Neill, M., Howie, J., Samson, J., Watt, S., Murray, K., McLean, D., Leslie, N. R., Safrany, S. T., Ferguson, M. J., Peters, J. A., Prescott, A. R., Box, G., Hayes, A., Nutley, B., Raynaud, F., Downes, C. P., Lambert, J. J., Thompson, A. M., and Eccles, S. (2004) Small molecule antagonists of the sigma-1 receptor cause selective release of the death program in tumor and self-reliant cells and inhibit tumor growth in vitro and in vivo. Cancer Res. 64, 4875-4886
17. Hanner, M., Moebius, F. F., Flandorfer, A., Knaus, H.-G., Striessnig, J., Kempner, E., and Glossmann, H. (1996) Purification, molecular cloning, and the expression of the mammalian sigma-1 binding site. Proc. Natl. Acad. Sci. U.S.A. 93, 8072-8077
18. 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
19. Balasuriya, D., Stewart, A. P., and Edwardson, J. M. (2013) The σ-1 receptor interacts directly with GluNl but not GluN2A in the GluN1/ GluN2A NMDA receptor. J. Neurosci. 33, 18219-18224
20. Kourrich, S., Hayashi, T., Chuang, J. Y., Tsai, S. Y., Su, T.-P., and Bonci, A. (2013) Dynamic interaction between sigma-1 receptor and Kv1.2 shapes neuronal and behavioral responses to cocaine. Cell 152, 236-247
21. 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 σ 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
22. Palmer, C. P., Mahen, R., Schnell, E., Djamgoz, M. B., and Aydar, E. (2007) σ-1 receptors bind cholesterol and remodel lipid rafts in breast cancer cell lines. Cancer Res. 67, 11166-11175
23. Fontanilla, D., Johannessen, M., Hajipour, A. R., Cozzi, N. V., Jackson, M. B., and Ruoho, A. E. (2009) The hallucinogen N,N-dimethyl-tryptamine (DMT) is an endogenous sigma-1 receptor regulator. Science 323, 934-937
24. Hayashi, T., and Su, T.-P. (2003) Intracellular dynamics of sigma-1 receptors (sigma-1 binding sites) in NG108-15 cells. J. Pharmacol. Exp. Ther. 306, 726-733
25. Johannessen, M., Ramachandran, S., Riemer, L., Ramos-Serrano, A., Ruoho, A. E., and Jackson, M. B. (2009) Voltage-gated sodium channel modulation by σ-receptor in cardiac myocytes and heterologous systems. Am. J. Physiol. Cell Physiol. 296, C1049-C1057
26. Johannessen, M., Fontanilla, D., Mavlyutov, T., Ruoho, A. E., and Jackson, M. B. (2011) Antagonist action of progesterone at σ-receptors in the modulation of voltage-gated sodium channels. Am. J. Physiol. Cell Physiol. 300, C328-C337
27. Tchedre, K. T., Huang, R. Q., Dibas, A., Krishnamoorthy, R. R., Dillon, G. H., and Yorio, T. (2008) Sigma-1 receptor regulation of voltage-gated calcium channels involves a direct interaction. Invest. Ophthalmol. Vis. Sci. 49, 4993-5002
28. Zhang, H., and Cuevas, J. (2002) Sigma receptors inhibit high-voltage-activated calcium channels in rat sympathetic and parasympathetic neurons. J. Neurophysiol. 87, 2867-2879
29. Zhang, H., and Cuevas, J. (2005) σ receptor activation blocks potassium channels and depresses neuroexcitability in rat intracardiac neurons. J. Pharmacol. Exp. Ther. 313, 1387-1396
30. Kinoshita, M., Matsuoka, Y., Suzuki, T., Mirrielees, J., and Yang, J. (2012) The sigma-1 receptor alters the kinetics of Kv1.3 voltage gated potassium channels but not the sensitivity to receptor ligands. Brain Res. 1452, 1-9
31. Monnet, F. P., Debonnel, G., Junien, J. L., and De Montigny, C. (1990) N-Methyl-D-aspartate-induced neuronal activation is selectively modulated by sigma receptors. Eur. J. Pharmacol. 179, 441-445
32. 2+ mobilization by N-methyl-D-aspartate in primary culture of rat frontal cortical neurons. J. Pharmacol. Exp. Ther. 275, 207-214
33. Kume, T., Nishikawa, H., Taguchi, R., Hashino, A., Katsuki, H., Kaneko, S., Minami, M., Satoh, M., and Akaike, A. (2002) Antagonism of NMDA receptors by sigma receptor ligands attenuates chemical ischemia-induced neuronal death in vitro. Eur. J. Pharmacol. 455, 91-100
34. 2+ influx in rat cortical neurons. J. Pharmacol. Exp. Ther. 327, 491-502
35. + channels in rat neurohypophysial terminals requires neither G-proteins nor ATP. J. Physiol. 526, 527-539
36. 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
37. + channel with 4-fold symmetry. J. Biol. Chem. 287, 37021-37029
38. Pabba, M., Wong, A. Y., Ahlskog, N., Hristova, E., Biscaro, D., Nassrallah, W., Ngsee, J. K., Snyder, M., Beique, J. C., and Bergeron, R. (2014) NMDA receptors are upregulated and trafficked to the plasma membrane after sigma-1 receptor activation in the rat hippocampus. J. Neurosci. 34, 11325-11338
39. Warmke, J. W., and Ganetzky, B. (1994) A family of potassium channel genes related to EAG in Drosophila and mammals. Proc. Natl. Acad. Sci. U.S.A. 91, 3438-3442
40. Kr potassium channel. Cell 81, 299-307
41. Trudeau, M. C., Warmke, J. W., Ganetzky, B., and Robertson, G. A. (1995) HERG, a human inward rectifier in the voltage-gated potassium channel family. Science 269, 92-95
42. Sanguinetti, M. C., and Tristani-Firouzi, M. (2006) hERG potassium channels and cardiac arrhythmia. Nature 440, 463-469
43. + channels: structure, function, and clinical significance. Physiol. Rev. 92, 1393-1478
44. Curran, M. E., Splawski, I., Timothy, K. W., Vincent, G. M., Green, E. D., Keating, M. T. (1995) A molecular basis for cardiac arrhythmia: HERG mutations cause long QT syndrome. Cell 80, 795-803
45. Zhou, Z., Gong, Q., Epstein, M. L., and January, C. T. (1998) HERG channel dysfunction in human long QT syndrome: intracellular transport and functional defects. J. Biol. Chem. 273, 21061-21066
46. Huffaker, S. J., Chen, J., Nicodemus, K. K., Sambataro, F., Yang, F., Mattay, V., Lipska, B. K., Hyde, T. M., Song, J., Rujescu, D., Giegling, I., Mayilyan, K., Proust, M. J., Soghoyan, A., Caforio, G., Callicott, J. H., Bertolino, A., Meyer-Lindenberg, A., Chang, J., Ji, Y., Egan, M. F., Goldberg, T. E., Kleinman, J. E., Lu, B., and Weinberger, D. R. (2009) A primate-specific, brain isoform of KCNH2 affects cortical physiology, cognition, and neuronal repolarization and risk of schizophrenia. Nat. Med. 15, 509-518
47. Farrelly, A. M., Ro, S., Callaghan, B. P., Khoyi, M. A., Fleming, N., Horowitz, B., Sanders, K. M., and Keef, K. D. (2003) Expression and function of KCNH2 (HERG) in the human jejunum. Am. J. Physiol. Gastrointest. Liver Physiol. 284, G883-G895
48. + channels in firing and release. FASEB J. 14, 2601-2610
49. + channel for a macromolecular signaling complex in acute myeloid leukemia: role in cell migration and clinical outcome. Blood 110, 1238-1250
50. Pillozzi, S., Masselli, M., De Lorenzo, E., Accordi, B., Cilia, E., Crociani, O., Amedei, A., Veltroni, M., D'Amico, M., Basso, G., Becchetti, A., Campana, D., and Arcangeli, A. (2011) Chemotherapy resistance in acute lymphoblastic leukemia requires hERG1 channels and is overcome by hERG1 blockers. Blood 117, 902-914
51. Crottès, D., Martial, S., Rapetti-Mauss, R., Pisani, D. F., Loriol, C., Pellissier, B., Martin, P., Chevet, E., Borgese, F., and Soriani, O. (2011) Sigma-1 receptor protein regulates hERG channel expression through a post-translational mechanism in leukemic cells. J. Biol. Chem. 286, 27947-27958
52. Albagli-Curiel, O., Lécluse, Y., Pognonec, P., Boulukos, K. E., and Martin, P. (2007) A new generation of pPRIG-based retroviral vectors. BMC Bio- technol. 7, 85
53. Söderberg, O., Gullberg, M., Jarvius, M., Ridderstråle, K., Leuchowius, K.-J., Jarvius, J., Wester, K., Hydbring, P., Bahram, F., Larsson, L. G., and Landegren, U. (2006) Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat. Methods 3, 995-1000
54. Schneider, S. W., Lärmer, J., Henderson, R. M., and Oberleithner, H. (1998) Molecular weights of individual proteins correlate with molecular volumes measured by atomic force microscopy. Pflügers Arch. 435, 362-367
55. Scott, D. W. (1979) On optimal and data-based histograms. Biometrika 66, 605-610
56. Welch, B. L. (1947) The generalisation of student's problems when several different population variances are involved. Biometrika 34, 28-35
57. Maurel, D., Kniazeff, J., Mathis, G., Trinquet, E., Pin, J.P., and Ansan ay, H. (2004) Cell surface detection of membrane protein interaction with homogeneous time-resolved fluorescence resonance energy transfer technology. Anal. Biochem. 329, 253-262
58. Los, G. V., Encell, L. P., McDougall, M. G., Hartzell, D. D., Karassina, N., Zimprich, C., Wood, M. G., Learish, R., Ohana, R. F., Urh, M., Simpson, D., Mendez, J., Zimmerman, K., Otto, P., Vidugiris, G., Zhu, J., Dar zins, A., Klaubert, D. H., Bulleit, R. F., and Wood, K. V. (2008) HaloTag: a novel protein labeling technology for cell imaging and protein analysis. ACS Chem. Biol. 6, 373-382
59. Maurice, T., and Su, T.-P. (2009) The pharmacology of sigma-1 receptors. Pharmacol. Ther. 124, 195-206
60. Rodal, S. K., Skretting, G., Garred, O., Vilhardt, F., van Deurs, B., and Sandvig, K. (1999) Extraction of cholesterol with methyl-ß-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol. Biol. Cell 10, 961-974
61. Phartiyal, P., Sale, H., Jones, E. M., Robertson, G. A. (2008) Endoplasmic reticulum retention and rescue by heteromeric assembly regulate human ERG 1a/1b surface channel composition. J. Biol. Chem. 283, 3702-3707
62. Ficker, E., Dennis, A. T., Wang, L., and Brown, A. M. (2003) Role of the cytosolic chaperones Hsp70 and Hsp90 in maturation of the cardiac potassium channel hERG. Circ. Res. 92, e87-e100
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. Navarro, G., Moreno, E., Aymerich, M., Marcellino, D., McCormick, P. J., Mallol, J., Cortés, A., Casadó, V., Canela, E. I., Ortiz, J., Fux e, K., Lluís, C., Ferré, S., and Franco, R. (2010) Direct involvement of σ-1 receptors in the dopamine D1 receptor-mediated effects of cocaine. Proc. Natl. Acad. Sci. U.S.A. 107, 18676-18681
65. Navarro, G., Moreno, E., Bonaventura, J., Brugarolas, M., Farré, D., Aguinaga, D., Mallol, J., Cortés, A., Casado, V., Lluís, C., Ferre, S., Franco, R., Canela, E., and McCormick, P. J. (2013) Cocaine inhibits dopamine D2 receptor signaling via sigma-1-D2 receptor heteromers. PLoS One 8, e61245