Modulation of ER stress and apoptosis by endoplasmic reticulum calcium leak via translocon during unfolded protein response: Involvement of GRP78

FASEB Journal

Volumn 27, Issue 4, 2013, Pages 1600-1609

  Hammadi, Mehdi ^g   Oulidi, Agathe ^a   Gackière, Florian ^b,c   Katsogiannou, Maria ^d,e,f   Slomianny, Christian ^a   Roudbaraki, Morad ^a   Dewailly, Etienne ^a   Delcourt, Philippe ^a   Lepage, Gilbert ^a   Lotteau, Sabine ^h   Ducreux, Sylvie ^h   Prevarskaya, Natalia ^a   Van Coppenolle, Fabien ^h  

^a Université des Sciences et Technologies de Lille   (France)

^b AIX MARSEILLE UNIVERSITÉ   (France)

^c CNRS   (France)

^d AIX MARSEILLE UNIVERSITY   (France)

^e AIX MARSEILLE UNIVERSITY   (France)

^f INSTITUT PAOLI CALMETTES   (France)

^g Université Picardie Jules Vernes   (France)

^h UNIVERSITÉ LYON 1   (France)

Author keywords

Bip; Cancer

Indexed keywords

ANISOMYCIN; GLUCOSE REGULATED PROTEIN 78; PUROMYCIN; TRANSLOCON;

APOPTOSIS; ARTICLE; CALCIUM DEPLETION; CELL STRAIN LNCAP; CELL SURVIVAL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; ION PERMEABILITY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; UNFOLDED PROTEIN RESPONSE;

ANISOMYCIN; APOPTOSIS; CALCIUM; CALCIUM CHANNELS; CELLS, CULTURED; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HEAT-SHOCK PROTEINS; HOMEOSTASIS; HUMANS; PUROMYCIN; UNFOLDED PROTEIN RESPONSE;

EID: 84875608277     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-218875     Document Type: Article

References (71)

1. Argos, P., Rao, J. K., and Hargrave, P. A. (1982) Structural prediction of membrane-bound proteins. Eur. J. Biochem. 128, 565-575.
2. Baldwin, J. M., Schertler, G. F., and Unger, V. M. (1997) An alpha-carbon template for the transmembrane helices in the rhodopsin family of G-protein-coupled receptors. J. Mol. Biol. 272, 144-164.
3. Unger, V. M., Hargrave, P. A., Baldwin, J. M., and Schertler, G. F. (1997) Arrangement of rhodopsin transmembrane alphahelices. Nature 389, 203-206.
4. 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.
5. Choe, H. W., Kim, Y. J., Park, J. H., Morizumi, T., Pai, E. F., Krauss, N., Hofmann, K. P., Scheerer, P., and Ernst, O. P. (2011) Crystal structure of metarhodopsin II. Nature 471, 651-655.
6. Park, J. H., Scheerer, P., Hofmann, K. P., Choe, H. W., and Ernst, O. P. (2008) Crystal structure of the ligand-free G-protein- coupled receptor opsin. Nature 454, 183-187.
7. 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. USA. 103, 16123-16128.
8. Nakamichi, H., and Okada, T. (2006) Local peptide movement in the photoreaction intermediate of rhodopsin. Proc. Natl. Acad. Sci. USA. 103, 12729-12734.
9. Deupi, X., Edwards, P., Singhal, A., Nickle, B., Oprian, D., Schertler, G., and Standfuss, J. (2012) Stabilized G protein binding site in the structure of constitutively active metarhodopsin- II. Proc. Natl. Acad. Sci. USA. 109, 119-124.
10. Lebon, G., Warne, T., and Tate, C. G. (2012) Agonist-bound structures of G protein-coupled receptors. Curr. Opin. Struct. Biol. 22, 482-490.
11. Katritch, V., Cherezov, V., and Stevens, R. C. (2012) Diversity and modularity of G protein-coupled receptor structures. Trend Pharmacol. Sci. 33, 17-27.
12. Palczewski, K. (2010) Oligomeric forms of G protein-coupled receptors (GPCRs). Trend Biochem. Sci. 35, 595-600.
13. Fotiadis, D., Liang, Y., Filipek, S., Saperstein, D. A., Engel, A., and Palczewski, K. (2003) Atomic-force microscopy: rhodopsin dimers in native disc membranes. Nature 421, 127-128.
14. Ianoul, A., Grant, D. D., Rouleau, Y., Bani-Yaghoub, M., Johnston, L. J., and Pezacki, J. P. (2005) Imaging nanometer domains of beta-adrenergic receptor complexes on the surface of cardiac myocytes. Nat. Chem. Biol. 1, 196-202.
15. Kniazeff, J., Prezeau, L., Rondard, P., Pin, J. P., and Goudet, C. (2011) Dimers and beyond: the functional puzzles of class C GPCRs. Pharmacol. Ther. 130, 9-25.
16. Bayburt, T. H., Leitz, A. J., Xie, G., Oprian, D. D., and Sligar, S. G. (2007) Transducin activation by nanoscale lipid bilayers containing one and two rhodopsins. J. Biol. Chem. 282, 14875- 14881.
17. Whorton, M. R., Jastrzebska, B., Park, P. S., Fotiadis, D., Engel, A., Palczewski, K., and Sunahara, R. K. (2008) Efficient coupling of transducin to monomeric rhodopsin in a phospholipid bilayer. J. Biol. Chem. 283, 4387-4394.
18. Lambert, N. A. (2010) GPCR dimers fall apart. Sci. Signal. 3, pe12.
19. Rivero-Muller, A., Chou, Y. Y., Ji, I., Lajic, S., Hanyaloglu, A. C., Jonas, K., Rahman, N., Ji, T. H., and Huhtaniemi, I. (2010) Rescue of defective G protein-coupled receptor function in vivo by intermolecular cooperation. Proc. Natl. Acad. Sci. USA. 107, 2319-2324.
20. Zhang, N., Kolesnikov, A.V., Jastrzebska, B., Mustafi, D., Sawada, O., Maeda, T., Genoud, C., Engel, A., Kefalov, V.J., and Palczewski, K. (2013) Knock-in E150K opsin mutant mice, a model for autosomal recessive retinitis pigmentosa, exhibit structural disorganization of photoreceptor internal membranes. J. Clin. Invest. 123, 121-137.
21. Jastrzebska, B., Ringler, P., Lodowski, D. T., Moiseenkova-Bell, V., Golczak, M., Muller, S. A., Palczewski, K., and Engel, A. (2011) Rhodopsin-transducin heteropentamer: three-dimensional structure and biochemical characterization. J. Struct. Biol. 176, 387-394.
22. Krebs, A., Villa, C., Edwards, P. C., and Schertler, G. F. (1998) Characterisation of an improved two-dimensional p22121 crystal from bovine rhodopsin. J. Mol. Biol. 282, 991-1003.
23. Park, P. S., Lodowski, D. T., and Palczewski, K. (2008) Activation of G protein-coupled receptors: beyond two-state models and tertiary conformational changes. Annu. Rev. Pharmacol. Toxicol. 48, 107-141.
24. Jastrzebska, B., Golczak, M., Fotiadis, D., Engel, A., and Palczewski, K. (2009) Isolation and functional characterization of a stable complex between photoactivated rhodopsin and the G protein, transducin. FASEB J. 23, 371-381.
25. Bulenger, S., Marullo, S., and Bouvier, M. (2005) Emerging role of homo- and heterodimerization in G-protein-coupled receptor biosynthesis and maturation. Trends Pharmacol. Sci. 26, 131-137.
26. Fotiadis, D., Jastrzebska, B., Philippsen, A., Muller, D. J., Palczewski, K., and Engel, A. (2006) Structure of the rhodopsin dimer: a working model for G-protein-coupled receptors. Curr. Opin. Struct. Biol. 16, 252-259.
27. Palczewski, K. (2006) G protein-coupled receptor rhodopsin. Annu. Rev. Biochem. 75, 743-767.
28. Okada, T., Ernst, O. P., Palczewski, K., and Hofmann, K. P. (2001) Activation of rhodopsin: new insights from structural and biochemical studies. Trends Biochem. Sci. 26, 318-324.
29. Spalink, J. D., Reynolds, A. H., Rentzepis, P. M., Sperling, W., and Applebury, M. L. (1983) Bathorhodopsin intermediates from 11-cis-rhodopsin and 9-cis-rhodopsin. Proc. Natl. Acad. Sci. USA. 80, 1887-1891.
30. Bornancin, F., Pfister, C., and Chabre, M. (1989) The transitory complex between photoexcited rhodopsin and transducin. Reciprocal interaction between the retinal site in rhodopsin and the nucleotide site in transducin. Eur. J. Biochem. 184, 687-698.
31. Vahedi-Faridi, A., Jastrzebska, B., Palczewski, K., and Engel, A. (2012) 3D imaging and quantitative analysis of small solubilized membrane proteins and their complexes by transmission electron microscopy. [E-pub ahead of print] J. Electron Microsc. doi: 10.1093/jmicro/dfs091.
32. Liang, Y., Fotiadis, D., Filipek, S., Saperstein, D. A., Palczewski, K., and Engel, A. (2003) Organization of the G protein-coupled receptors rhodopsin and opsin in native membranes. J. Biol. Chem. 278, 21655-21662.
33. Papermaster, D. S. (1982) Preparation of retinal rod outer segments. Methods Enzymol. 81, 48-52.
34. Okada, T., Tsujimoto, R., Muraoka, M., and Funamoto, C. (2005) Methods and results in X-ray crystallography of bovine rhodopsin. In G Protein-Coupled Receptors: Structure, Function, andLigand Screening (Haga, T., ed) pp. 245-261, CRC Press, Boca Raton, FL, USA.
35. Wald, G., and Brown, P. K. (1953) The molecular excitation of rhodopsin. J. Gen. Physiol. 37, 189-200.
36. Goc, A., Angel, T. E., Jastrzebska, B., Wang, B., Wintrode, P. L., and Palczewski, K. (2008) Different properties of the native and reconstituted heterotrimeric G protein transducin. Biochemistry 47, 12409-12419.
37. 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.
38. Surya, A., Foster, K. W., and Knox, B. E. (1995) Transducin activation by the bovine opsin apoprotein. J. Biol. Chem. 270, 5024-5031.
39. Kito, Y., Suzuki, T., Azuma, M., and Sekoguti, Y. (1968) Absorption spectrum of rhodopsin denatured with acid. Nature 218, 955-957.
40. Kropf, A., and Hubbard, R. (1970) The photoisomerization of retinal. Photochem. Photobiol. 12, 249-260.
41. Van Hooser, J. P., Garwin, G. G., and Saari, J. C. (2000) Analysis of visual cycle in normal and transgenic mice. Methods Enzymol. 316, 565-575.
42. Garwin, G. G., and Saari, J. C. (2000) High-performance liquid chromatography analysis of visual cycle retinoids. Methods Enzymol. 316, 313-324.
43. Bownds, D., and Wald, G. (1965) Reaction of the rhodopsin chromophore with sodium borohydride. Nature 205, 254-257.
44. Jastrzebska, B., Palczewski, K., and Golczak, M. (2011) Role of bulk water in hydrolysis of the rhodopsin chromophore. J. Biol. Chem. 286, 18930-18937.
45. Wald, G., and Hubbard, R. (1957) Visual pigment of a decapod crustacean: the lobster. Nature 180, 278-280.
46. Heck, M., Schadel, S. A., Maretzki, D., and Hofmann, K. P. (2003) Secondary binding sites of retinoids in opsin: characterization and role in regeneration. Vision Res. 43, 3003-3010.
47. Schadel, S. A., Heck, M., Maretzki, D., Filipek, S., Teller, D. C., Palczewski, K., and Hofmann, K. P. (2003) Ligand channeling within a G-protein-coupled receptor. The entry and exit of retinals in native opsin. J. Biol. Chem. 278, 24896-24903.
48. Han, Y., Moreira, I. S., Urizar, E., Weinstein, H., and Javitch, J. A. (2009) Allosteric communication between protomers of dopamine class A GPCR dimers modulates activation. Nat. Chem. Biol. 5, 688-695.
49. Damian, M., Martin, A., Mesnier, D., Pin, J. P., and Baneres, J. L. (2006) Asymmetric conformational changes in a GPCR dimer controlled by G-proteins. EMBO J. 25, 5693-5702.
50. Maurice, P., Kamal, M., and Jockers, R. (2011) Asymmetry of GPCR oligomers supports their functional relevance. Trends Pharmacol. Sci. 32, 514-520.
51. Bownds, D. (1967) Site of attachment of retinal in rhodopsin. Nature 216, 1178-1181.
52. Matthews, R. G., Hubbard, R., Brown, P. K., and Wald, G. (1963) Tautomeric forms of metarhodopsin. J. Gen. Physiol. 47, 215-240.
53. Murakami, M., and Kouyama, T. (2008) Crystal structure of squid rhodopsin. Nature 453, 363-367.
54. Lambright, D. G., Sondek, J., Bohm, A., Skiba, N. P., Hamm, H. E., and Sigler, P. B. (1996) The 2.0 A crystal structure of a heterotrimeric G protein. Nature 379, 311-319.
55. Granzin, J., Wilden, U., Choe, H. W., Labahn, J., Krafft, B., and Buldt, G. (1998) X-ray crystal structure of arrestin from bovine rod outer segments. Nature 391, 918-921.
56. Lodowski, D. T., Tesmer, V. M., Benovic, J. L., and Tesmer, J. J. (2006) The structure of G protein-coupled receptor kinase (GRK)-6 defines a second lineage of GRKs. J. Biol. Chem. 281, 16785-16793.
57. Singh, P., Wang, B., Maeda, T., Palczewski, K., and Tesmer, J. J. (2008) Structures of rhodopsin kinase in different ligand states reveal key elements involved in G protein-coupled receptor kinase activation. J. Biol. Chem. 283, 14053-14062.
58. Tateyama, M., Abe, H., Nakata, H., Saito, O., and Kubo, Y. (2004) Ligand-induced rearrangement of the dimeric metabotropic glutamate receptor 1alpha. Nat. Struct. Mol. Biol. 11, 637-642.
59. Kunishima, N., Shimada, Y., Tsuji, Y., Sato, T., Yamamoto, M., Kumasaka, T., Nakanishi, S., Jingami, H., and Morikawa, K. (2000) Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor. Nature 407, 971-977.
60. Kaupmann, K., Malitschek, B., Schuler, V., Heid, J., Froestl, W., Beck, P., Mosbacher, J., Bischoff, S., Kulik, A., Shigemoto, R., Karschin, A., and Bettler, B. (1998) GABA(B)-receptor subtypes assemble into functional heteromeric complexes. Nature 396, 683-687.
61. Jones, K. A., Borowsky, B., Tamm, J. A., Craig, D. A., Durkin, M. M., Dai, M., Yao, W. J., Johnson, M., Gunwaldsen, C., Huang, L. Y., Tang, C., Shen, Q., Salon, J. A., Morse, K., Laz, T., Smith, K. E., Nagarathnam, D., Noble, S. A., Branchek, T. A., and Gerald, C. (1998) GABA(B) receptors function as a heteromeric assembly of the subunits GABA(B)R1 and GABA(B)R2. Nature 396, 674-679.
62. White, J. H., Wise, A., Main, M. J., Green, A., Fraser, N. J., Disney, G. H., Barnes, A. A., Emson, P., Foord, S. M., and Marshall, F. H. (1998) Heterodimerization is required for the formation of a functional GABA(B) receptor. Nature 396, 679- 682.
63. Chandrashekar, J., Hoon, M. A., Ryba, N. J., and Zuker, C. S. (2006) The receptors and cells for mammalian taste. Nature 444, 288-294.
64. Huang, A. L., Chen, X., Hoon, M. A., Chandrashekar, J., Guo, W., Trankner, D., Ryba, N. J., and Zuker, C. S. (2006) The cells and logic for mammalian sour taste detection. Nature 442, 934-938.
65. Filipek, S., Krzysko, K. A., Fotiadis, D., Liang, Y., Saperstein, D. A., Engel, A., and Palczewski, K. (2004) A concept for G protein activation by G protein-coupled receptor dimers: the transducin/rhodopsin interface. Photochem. Photobiol. Sci. 3, 628-638.
66. Modzelewska, A., Filipek, S., Palczewski, K., and Park, P. S. (2006) Arrestin interaction with rhodopsin: conceptual models. Cell Biochem. Biophys. 46, 1-15.
67. Orban, T., Jastrzebska, B., Gupta, S., Wang, B., Miyagi, M., Chance, M. R., and Palczewski, K. (2012) Conformational dynamics of activation for the pentameric complex of dimeric G protein-coupled receptor and heterotrimeric G protein. Structure 20, 826-840.
68. Rasmussen, S. G., DeVree, B. T., Zou, Y., Kruse, A. C., Chung, K. Y., Kobilka, T. S., Thian, F. S., Chae, P. S., Pardon, E., Calinski, D., Mathiesen, J. M., Shah, S. T., Lyons, J. A., Caffrey, M., Gellman, S. H., Steyaert, J., Skiniotis, G., Weis, W. I., Sunahara, R. K., and Kobilka, B. K. (2011) Crystal structure of the beta2 adrenergic receptor-Gs protein complex. Nature 477, 549-555.
69. Fanelli, F., and Dell'orco, D. (2008) Dark and photoactivated rhodopsin share common binding modes to transducin. FEBS Lett. 582, 991-996.
70. Neri, M., Vanni, S., Tavernelli, I., and Rothlisberger, U. (2010) Role of aggregation in rhodopsin signal transduction. Biochemistry 49, 4827-4832.
71. Filizola, M., Wang, S. X., and Weinstein, H. (2006) Dynamic models of G-protein coupled receptor dimers: indications of asymmetry in the rhodopsin dimer from molecular dynamics simulations in a POPC bilayer. J. Comput. Aided Mol. Des. 20, 405-416.