The Endoplasmic Reticulum Ca2+-pump SERCA2b Interacts with G Protein-coupled Receptors and Enhances their Expression at the Cell Surface

Journal of Molecular Biology

Volumn 371, Issue 3, 2007, Pages 622-638

  Tuusa, Jussi T ^a   Markkanen, Piia M H ^a   Apaja, Pirjo M ^a   Hakalahti, Anna E ^a   Petäjä Repo, Ulla E ^a  

^a UNIVERSITY OF OULU   (Finland)

Author keywords

calcium; endoplasmic reticulum; G protein coupled receptor; protein protein interaction; SERCA

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); CALCIMYCIN; CALNEXIN; DELTA OPIATE RECEPTOR; G PROTEIN COUPLED RECEPTOR; LUTEINIZING HORMONE; SARCOPLASMIC RETICULUM CALCIUM ATPASE 2B; UNCLASSIFIED DRUG; ATP2A2 PROTEIN, HUMAN; LUTEINIZING HORMONE RECEPTOR; PROTEIN PRECURSOR; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; THAPSIGARGIN;

ARTICLE; BIOGENESIS; CALCIUM HOMEOSTASIS; CELL SURFACE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; ANIMAL; CELL LINE; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ACTIVATION; ENZYME SPECIFICITY; ENZYMOLOGY; FEMALE; METABOLISM; OVARY; PREGNANCY; PROTEIN BINDING; RAT;

RATTUS;

ANIMALS; CALNEXIN; CELL LINE; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; FEMALE; HUMANS; IMMUNOPRECIPITATION; OVARY; PREGNANCY; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN PRECURSORS; RATS; RECEPTORS, LH; RECEPTORS, OPIOID, DELTA; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SUBSTRATE SPECIFICITY; THAPSIGARGIN;

EID: 34447633217     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.02.108     Document Type: Article

References (57)

1. Ellgaard L., and Helenius A. ER quality control: towards an understanding at the molecular level. Curr. Opin. Cell Biol. 13 (2001) 431-437
2. Berridge M.J. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32 (2002) 235-249
3. Brostrom M.A., and Brostrom C.O. Calcium dynamics and endoplasmic reticular function in the regulation of protein synthesis: implications for cell growth and adaptability. Cell Calcium 34 (2003) 345-363
4. 2+ signaling and calcium binding chaperones of the endoplasmic reticulum. Cell Calcium 32 (2002) 269-278
5. Paschen W. Dependence of vital cell function on endoplasmic reticulum calcium levels: implications for the mechanisms underlying neuronal cell injury in different pathological states. Cell Calcium 29 (2001) 1-11
6. Wuytack F., Raeymaekers L., and Missiaen L. Molecular physiology of the SERCA and SPCA pumps. Cell Calcium 32 (2002) 279-305
7. 2+ ATPase 2 (SERCA2) activity: cell biological implications. Cell Calcium 38 (2005) 291-302
8. 2+-ATPase isoform 2 (SERCA2) gene. J. Biol. Chem. 274 (1999) 2556-2562
9. Caspersen C., Pedersen P.S., and Treiman M. The sarco/endoplasmic reticulum calcium-ATPase 2b is an endoplasmic reticulum stress-inducible protein. J. Biol. Chem. 275 (2000) 22363-22372
10. 2+ and other cation-transporting ATPases using an oligonucleotide probe derived from the ATP-binding site. J. Biol. Chem. 263 (1988) 15032-15040
11. 2+-ATPase gene. J. Biol. Chem. 263 (1988) 15024-15031
12. Gélébart P., Martin V., Enouf J., and Papp B. Identification of a new SERCA2 splice variant regulated during monocytic differentiation. Biochem. Biophys. Res. Commun. 303 (2003) 676-684
13. John L.M., Lechleiter J.D., and Camacho P. Differential modulation of SERCA2 isoforms by calreticulin. J. Cell Biol. 142 (1998) 963-973
14. 2+ oscillations via an interaction with SERCA2b. J. Cell Biol. 149 (2000) 1235-1248
15. 2+-dependent redox modulation of SERCA 2b by ERp57. J. Cell Biol. 164 (2004) 35-46
16. Karnik S.S., Gogonea C., Patil S., Saad Y., and Takezako T. Activation of G-protein-coupled receptors: a common molecular mechanism. Trends Endocrinol. Metab. 14 (2003) 431-437
17. Petäjä-Repo U., and Bouvier M. Folding and maturation of GPCRs. The effect of pharmacological chaperones. In: Devi L.A. (Ed). Contemporary Clinical Neuroscience, The G Protein-Coupled Receptors Handbook (2005), Humana Press, Totowa, NJ 71-93
18. Pietilä E.M., Tuusa J.T., Apaja P.M., Aatsinki J.T., Hakalahti A.E., Rajaniemi H.J., and Petäjä-Repo U.E. Inefficient maturation of the rat luteinizing hormone receptor. A putative way to regulate receptor numbers at the cell surface. J. Biol. Chem. 280 (2005) 26622-26629
19. Apaja P.M., Aatsinki J.T., Rajaniemi H.J., and Petäjä-Repo U.E. Expression of the mature luteinizing hormone receptor in rodent urogenital and adrenal tissues is developmentally regulated at a posttranslational level. Endocrinology 146 (2005) 3224-3232
20. Morello J.P., Salahpour A., Petäjä-Repo U.E., Laperrière A., Lonergan M., Arthus M.F., et al. Association of calnexin with wild type and mutant AVPR2 that causes nephrogenic diabetes insipidus. Biochemistry 40 (2001) 6766-6775
21. Mizrachi D., and Segaloff D.L. Intracellularly located misfolded glycoprotein hormone receptors associate with different chaperone proteins than their cognate wild-type receptors. Mol. Endocrinol. 18 (2004) 1768-1777
22. 2+ regulation, and photoreceptor cell survival. Neuron 49 (2006) 229-241
23. Colley N.J., Baker E.K., Stamnes M.A., and Zuker C.S. The cyclophilin homolog ninaA is required in the secretory pathway. Cell 67 (1991) 255-263
24. McLatchie L.M., Fraser N.J., Main M.J., Wise A., Brown J., Thompson N., et al. RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature 393 (1998) 333-339
25. Leskelä, T. T., Markkanen, P. M. H., Pietilä, E. M., Tuusa, J. T. & Petäjä_Repo, U. E. (2007). Opioid receptor pharmacological chaperones act by binding and stabilizing newly synthesized receptors in the endoplasmic reticulum. J. Biol. Chem. In the Press.
26. Petäjä-Repo U.E., Hogue M., Laperrière A., Walker P., and Bouvier M. 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 (2000) 13727-13736
27. Petäjä-Repo U.E., Hogue M., Laperrière A., Bhalla S., Walker P., and Bouvier M. Newly synthesized human δ opioid receptors retained in the endoplasmic reticulum are retrotranslocated to the cytosol, deglycosylated, ubiquitinated, and degraded by the proteasome. J. Biol. Chem. 276 (2001) 4416-4423
28. Petäjä-Repo U.E., Hogue M., Leskelä T.T., Markkanen P.M.H., Tuusa J.T., and Bouvier M. Distinct subcellular localization for constitutive and agonist-modulated palmitoylation of the human δ opioid receptor. J. Biol. Chem. 281 (2006) 15780-15789
29. 2+-transport ATPase. Biochem. J. 264 (1989) 765-769
30. 2+ATPase 3 gene. J. Biol. Chem. 279 (2004) 24297-24306
31. Chandrasekera C.P., and Lytton J. Inhibition of human SERCA3 by PL/IM430. Molecular analysis of the interaction. J. Biol. Chem. 278 (2003) 12482-12488
32. 2+-ATPase. Calcium affinities and inhibitor effects. J. Biol. Chem. 266 (1991) 16050-16055
33. Petäjä-Repo U.E., Hogue M., Bhalla S., Laperrière A., Morello J.P., and Bouvier M. Ligands act as pharmacological chaperones and increase the efficiency of δ opioid receptor maturation. EMBO J. 21 (2002) 1628-1637
34. 2+ from the endoplasmic reticulum. Biochem. J. 370 (2003) 449-458
35. Di Jeso B., Formisano S., and Ulianich L. Perturbation of cellular calcium delays the secretion and alters the glycosylation of thyroglobulin in FRTL-5 cells. Biochem. Biophys. Res. Commun. 234 (1997) 133-136
36. Blobel G., and Dobberstein B. Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J. Cell Biol. 67 (1975) 835-851
37. Van den Berg B., Clemons Jr. W.M., Collinson I., Modis Y., Hartmann E., Harrison S.C., and Rapoport T.A. X-ray structure of a protein-conducting channel. Nature 427 (2004) 36-44
38. Ellgaard L., and Helenius A. Quality control in the endoplasmic reticulum. Nature Rev. Mol. Cell. Biol. 4 (2003) 181-191
39. Römisch K. Endoplasmic reticulum-associated degradation. Annu. Rev. Cell Dev. Biol. 21 (2005) 435-456
40. Lodish H.F., Kong N., and Wikström L. Calcium is required for folding of newly made subunits of the asialoglycoprotein receptor within the endoplasmic reticulum. J. Biol. Chem. 267 (1992) 12753-12760
41. Pittman D.D., Tomkinson K.N., and Kaufman R.J. Post-translational requirements for functional factor V and factor VIII secretion in mammalian cells. J. Biol. Chem. 269 (1994) 17329-17337
42. van Weering D.H.J., Moen T.C., Braakman I., Baas P.D., and Bos J.L. Expression of the receptor tyrosine kinase Ret on the plasma membrane is dependent on calcium. J. Biol. Chem. 273 (1998) 12077-12081
43. Egan M.E., Glöckner-Pagel J., Ambrose C., Cahill P.A., Pappoe L., Balamuth N., et al. Calcium-pump inhibitors induce functional surface expression of Delta F508-CFTR protein in cystic fibrosis epithelial cells. Nature Med. 8 (2002) 485-492
44. Delisle B.P., Anderson C.L., Balijepalli R.C., Anson B.D., Kamp T.J., and January C.T. Thapsigargin selectively rescues the trafficking defective LQT2 channels G601S and F805C. J. Biol. Chem. 278 (2003) 35749-35754
45. 2+ pump SERCA2b and is necessary for collagen type I synthesis. Mol. Cell. Biol. 24 (2004) 1758-1768
46. Rapoport T.A., Goder V., Heinrich S.U., and Matlack K.E. Membrane-protein integration and the role of the translocation channel. Trends Cell Biol. 14 (2004) 568-575
47. van Meer G. Lipid traffic in animal cells. Annu. Rev. Cell Biol. 5 (1989) 247-275
48. Le Gall S., Neuhof A., and Rapoport T. The endoplasmic reticulum membrane is permeable to small molecules. Mol. Biol. Cell 15 (2004) 447-455
49. Van Coppenolle F., Vanden Abeele F., Slomianny C., Flourakis M., Hesketh J., Dewailly E., and Prevarskaya N. Ribosome-translocon complex mediates calcium leakage from endoplasmic reticulum stores. J. Cell Sci. 117 (2004) 4135-4142
50. Tipper D.J., and Harley C.A. Yeast genes controlling responses to topogenic signals in a model transmembrane protein. Mol. Biol. Cell 13 (2002) 1158-1174
51. Imai Y., Soda M., Inoue H., Hattori N., Mizuno Y., and Takahashi R. An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of Parkin. Cell 105 (2001) 891-902
52. Rezgaoui M., Süsens U., Ignatov A., Gelderblom M., Glassmeier G., Franke I., et al. The neuropeptide head activator is a high-affinity ligand for the orphan G-protein-coupled receptor GPR37. J. Cell Sci. 119 (2006) 542-549
53. 2+ signaling in rotenone-induced apoptosis in human neuroblastoma SH-SY5Y cells. Neurosci. Letters 376 (2005) 127-132
54. Aatsinki J.T., and Rajaniemi H.J. An alternative use of basic pGEX vectors for producing N- and C-terminal fusion proteins for production and affinity purification of antibodies. Protein Expr. Purif. 40 (2005) 287-291
55. Apaja P.M., Tuusa J.T., Pietilä E.M., Rajaniemi H.J., and Petäjä-Repo U.E. Luteinizing hormone receptor ectodomain splice variant misroutes the full-length receptor into a subcompartment of the endoplasmic reticulum. Mol. Biol. Cell 17 (2006) 2243-2255
56. Blum H., Beier H., and Gross H.J. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8 (1987) 93-99
57. Shevchenko A., Wilm M., Vorm O., and Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68 (1996) 850-858