Human δ opioid receptor biogenesis is regulated via interactions with SERCA2b and calnexin

FEBS Journal

Volumn 277, Issue 13, 2010, Pages 2815-2829

  Tuusa, Jussi T ^a   Leskelä, Tarja T ^a   Petäjä Repo, Ulla E ^a  

^a UNIVERSITY OF OULU   (Finland)

Author keywords

Calnexin; Endoplasmic reticulum; G protein coupled receptor (GPCR); Opioid receptor; Sarco(endo)plasmic reticulum calcium ATPase (SERCA)

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; CALNEXIN; CHAPERONE; DELTA OPIATE RECEPTOR; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 2B; TRANSLOCON; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING;

ADENOSINE TRIPHOSPHATE; CALCIUM; CALNEXIN; HUMANS; RECEPTORS, OPIOID, DELTA; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

EID: 77953548554     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07699.x     Document Type: Article

References (43)

1. Brostrom MA Brostrom CO (2003) Calcium dynamics and endoplasmic reticular function in the regulation of protein synthesis: implications for cell growth and adaptability. Cell Calcium 34, 345-363.
2. Paschen W Mengesdorf T (2005) Endoplasmic reticulum stress response and neurodegeneration. Cell Calcium 38, 409-415.
3. 2+-ATPase (SERCA) 1 and 2 isoforms and characterization of Darier disease (SERCA2) mutants by steady-state and transient kinetic analyses. J Biol Chem 278, 47877-47889.
4. Hovnanian A (2004) Darier's disease: from dyskeratosis to endoplasmic reticulum calcium ATPase deficiency. Biochem Biophys Res Commun 322, 1237-1244.
5. Leinonen PT, Hägg PM, Peltonen S, Jouhilahti EM, Melkko J, Korkiamaki T, Oikarinen A Peltonen J (2009) Reevaluation of the normal epidermal calcium gradient, and analysis of calcium levels and ATP receptors in Hailey-Hailey and Darier epidermis. J Invest Dermatol 129, 1379-1387.
6. Kristiansen K (2004) Molecular mechanisms of ligand binding, signaling, and regulation within the superfamily of G-protein-coupled receptors: molecular modeling and mutagenesis approaches to receptor structure and function. Pharmacol Ther 103, 21-80.
7. Rapoport TA (2007) Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450, 663-669.
8. Ismail N, Crawshaw SG, Cross BCS, Haagsma AC High S (2008) Specific transmembrane segments are selectively delayed at the ER translocon during opsin biogenesis. Biochem J 411, 495-506.
9. Wilson CM, Kraft C, Duggan C, Ismail N, Crawshaw SG High S (2005) Ribophorin I associates with a subset of membrane proteins after their integration at the Sec61 translocon. J Biol Chem 280, 4195-4206.
10. Meacock SL, Lecomte FJL, Crawshaw SG High S (2002) Different transmembrane domains associate with distinct endoplasmic reticulum components during membrane integration of a polytopic protein. Mol Biol Cell 13, 4114-4129.
11. Sauri A, McCormick PJ, Johnson AE Mingarro I (2007) Sec61α and TRAM are sequentially adjacent to a nascent viral membrane protein during its ER integration. J Mol Biol 366, 366-374.
12. Fons RD, Bogert BA Hegde RS (2003) Substrate-specific function of the translocon-associated protein complex during translocation across the ER membrane. J Cell Biol 160, 529-539.
13. Helenius A Aebi M (2004) Roles of N-linked glycans in the endoplasmic reticulum. Annu Rev Biochem 73, 1019-1049.
14. Chevet E, Wong HN, Gerber D, Cochet C, Fazel A, Cameron PH, Gushue JN, Thomas DY Bergeron JJ (1999) Phosphorylation by CK2 and MAPK enhances calnexin association with ribosomes. EMBO J 18, 3655-3666.
15. 2+ oscillations via an interaction with SERCA2b. J Cell Biol 149, 1235-1248.
16. 2+-dependent redox modulation of SERCA 2b by ERp57. J Cell Biol 164, 35-46.
17. 2+ pump Serca2b and is necessary for collagen type I synthesis. Mol Cell Biol 24, 1758-1768.
18. 2+-pump SERCA2b Interacts with G protein-coupled receptors and enhances their expression at the cell surface. J Mol Biol 371, 622-638.
19. Apaja PM, Tuusa JT, Pietilä EM, Rajaniemi HJ Petäjä-Repo UE (2006) Luteinizing hormone receptor ectodomain splice variant misroutes the full-length receptor into a subcompartment of the endoplasmic reticulum. Mol Biol Cell 17, 2243-2255.
20. Leskelä TT, Markkanen PMH, Pietilä EM, Tuusa JT Petäjä-Repo UE (2007) Opioid receptor pharmacological chaperones act by binding and stabilizing newly synthesized receptors in the endoplasmic reticulum. J Biol Chem 282, 23171-23183.
21. Markkanen PMH Petäjä-Repo UE (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.
22. Leskelä TT, Markkanen PMH, Alahuhta IA, Tuusa JT Petaja- Repo UE (2009) Phe27Cys polymorphism alters the maturation and subcellular localization of the human δ opioid receptor. Traffic 10, 116-129.
23. Petäjä-Repo UE, Hogue M, Laperrière A, Walker P Bouvier M (2000) Export from the endoplasmic reticulum represents the limiting step in the maturation and cell surface expression of the human δ opioid receptor. J Biol Chem 275, 13727-13736.
24. Daniels R, Kurowski B, Johnson AE Hebert DN (2003) N-linked glycans direct the cotranslational folding pathway of influenza hemagglutinin. Mol Cell 11, 79-90.
25. Ahn W, Lee MG, Kim KH Muallem S (2003) Multiple effects of SERCA2b mutations associated with Darier's disease. J Biol Chem 278, 20795-20801.
26. John LM, Lechleiter JD Camacho P (1998) Differential modulation of SERCA2 isoforms by calreticulin. J Cell Biol 142, 963-973.
27. Suarez J, Gloss B, Belke DD, Hu Y, Scott B, Dieterle T, Kim YK, Valencik ML, McDonald JA Dillmann WH (2004) Doxycycline inducible expression of SERCA2a improves calcium handling and reverts cardiac dysfunction in pressure overload-induced cardiac hypertrophy. Am J Physiol Heart Circ Physiol 287, H2164 H2172.
28. Brockmeier A Williams DB (2006) Potent lectin-independent chaperone function of calnexin under conditions prevalent within the lumen of the endoplasmic reticulum. Biochemistry 45, 12906-12916.
29. Olesen C, Picard M, Winther AML, Gyrup C, Morth JP, Oxvig C, Møller JV Nissen P (2007) The structural basis of calcium transport by the calcium pump. Nature 450, 1036-1042.
30. Mueller B, Zhao M, Negrashov IV, Bennett R Thomas DD (2004) SERCA structural dynamics induced by ATP and calcium. Biochemistry 43, 12846-12854.
31. Jensen AM, Sørensen TL, Olesen C, Møller JV Nissen P (2006) Modulatory and catalytic modes of ATP binding by the calcium pump. EMBO J 25, 2305-2314.
32. 2+-ATPase. J Biol Chem 274, 25227-25236.
33. 2+ release. J Biol Chem 283, 14867-14882.
34. Wiseman RL, Powers ET, Buxbaum JN, Kelly JW Balch WE (2007) An adaptable standard for protein export from the endoplasmic reticulum. Cell 131, 809-821.
35. Means S, Smith AJ, Shepherd J, Shadid J, Fowler J, Wojcikiewicz RJH, Mazel T, Smith GD Wilson BS (2006) Reaction diffusion modeling of calcium dynamics with realistic ER geometry. Biophys J 91, 537-557.
36. Burdakov D, Petersen OH Verkhratsky A (2005) Intraluminal calcium as a primary regulator of endoplasmic reticulum function. Cell Calcium 38, 303-310.
37. 2+ oscillations. Biochem J 383, 353-360.
38. Van Coppenolle F, Vanden Abeele F, Slomianny C, Flourakis M, Hesketh J, Dewailly E Prevarskaya N (2004) Ribosome-translocon complex mediates calcium leakage from endoplasmic reticulum stores. J Cell Sci 117, 4135-4142.
39. 2+ ATPase). Mol Pharmacol 73, 1134-1140.
40. Mayer M, Reinstein J Buchner J (2003) Modulation of the ATPase cycle of BiP by peptides and proteins. J Mol Biol 330, 137-144.
41. Pitonzo D, Yang Z, Matsumura Y, Johnson AE Skach WR (2009) Sequence-specific retention and regulated integration of a nascent membrane protein by the endoplasmic reticulum Sec61 translocon. Mol Biol Cell 20, 685-698.
42. Pietilä EM, Tuusa JT, Apaja PM, Aatsinki JT, Hakalahti AE, Rajaniemi HJ Petäjä-Repo UE (2005) Inefficient maturation of the rat luteinizing hormone receptor. A putative way to regulate receptor numbers at the cell surface. J Biol Chem 280, 26622-26629.
43. 2+ ATPase 2 (SERCA2) activity: cell biological implications. Cell Calcium 38, 291-302.