Phe27Cys polymorphism alters the maturation and subcellular localization of the human δ opioid receptor

Traffic

Volumn 10, Issue 1, 2009, Pages 116-129

  Leskelä, Tarja T ^a   Markkanen, Piia M H ^a   Alahuhta, Ilkka A ^a   Tuusa, Jussi T ^a   Petäjä Repo, Ulla E ^a  

^a UNIVERSITY OF OULU   (Finland)

Author keywords

Biosynthesis; Endocytosis; Endoplasmic reticulum; ER quality control; ER associated degradation; Folding; G protein coupled receptor; Internalization; Opioid receptor; Pharmacological chaperone; Polymorphism; Trafficking

Indexed keywords

CYSTEINE; OPIATE ANTAGONIST; OPIATE RECEPTOR; PHENYLALANINE;

ARTICLE; BIOSYNTHESIS; CELL COMPARTMENTALIZATION; CELL FUNCTION; CELL LOSS; CELL MATURATION; CELL MEMBRANE TRANSPORT; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENETIC VARIABILITY; GOLGI COMPLEX; HETEROLOGOUS EXPRESSION; HUMAN; HUMAN CELL; INTERNALIZATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; SINGLE NUCLEOTIDE POLYMORPHISM;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CONSERVED SEQUENCE; CYSTEINE; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; HUMANS; KINETICS; MOLECULAR SEQUENCE DATA; PHENYLALANINE; POLYMORPHISM, GENETIC; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RECEPTORS, OPIOID, DELTA; SEQUENCE ALIGNMENT;

EID: 58149187864     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2008.00846.x     Document Type: Article

References (46)

1. Bjarnadóttir TK, Gloriam DE, Hellstrand SH, Kristiansson H, Fredriksson R, Schiöth HB. Comprehensive repertoire and phylogenetic analysis of the G protein-coupled receptors in human and mouse. Genomics 2006; 88: 263-273.
2. Marinissen MJ, Gutkind JS. G-protein-coupled receptors and signaling networks: Emerging paradigms. Trends Pharmacol Sci 2001; 22: 368-376.
3. Levoye A, Dam J, Ayoub MA, Guillaume JL, Jockers R. Do orphan G-protein-coupled receptors have ligand-independent functions? New insights from receptor heterodimers. EMBO Rep 2006; 7: 1094-1098.
4. Terrillon S, Bouvier M. Roles of G-protein-coupled receptor dimerization. EMBO Rep 2004; 5: 30-34.
5. Ulloa-Aguirre A, Janovick JA, Miranda AL, Conn PM. G-protein-coupled receptor trafficking: Understanding the chemical basis of health and disease. ACS Chem Biol 2006; 1: 631-638.
6. Minneman KP. Splice variants of G protein-coupled receptors. Mol Interv 2001; 1: 108-116.
7. Thompson MD, Burnham WM, Cole DEC. The G protein-coupled receptors: pharmacogenetics and disease. Crit Rev Clin Lab Sci 2005; 42: 311-392.
8. Insel PA, Tang CM, Hahntow I, Michel MC. Impact of GPCRs in clinical medicine: Monogenic diseases, genetic variants and drug targets. Biochim Biophys Acta 2007; 1768: 994-1005.
9. Waldhoer M, Bartlett SE, Whistler JL. Opioid receptors. Annu Rev Biochem 2004; 73: 953-990.
10. Mayer P, Höllt V. Allelic and somatic variations in the endogenous opioid system of humans. Pharmacol Ther 2001; 91: 167-177.
11. Lötsch J, Geisslinger G. Are μ-opioid receptor polymorphisms important for clinical opioid therapy? Trends Mol Med 2005; 11: 82-89.
12. Gelernter J, Kranzler HR. Variant detection at the δ opioid receptor (OPRD1) locus and population genetics of a novel variant affecting protein sequence. Hum Genet 2000; 107: 86-88.
13. Kim H, Neubert JK, San Miguel A, Xu K, Krishnaraju RK, Iadarola MJ, Goldman D, Dionne RA. Genetic influence on variability in human acute experimental pain sensitivity associated with gender, ethnicity and psychological temperament. Pain 2004; 109: 488-496.
14. Mayer P, Rochlitz H, Rauch E, Rommelspacher H, Hasse HE, Schmidt S, Höllt V. Association between a delta opioid receptor gene polymorphism and heroin dependence in man. Neuroreport 1997; 8: 2547-2550.
15. Bergen AW, van den Bree MBM, Yeager M, Welch R, Ganjei JK, Haque K, Bacanu S, Berrettini WH, Grice DE, Goldman D, Bulik CM, Klump K, Fichter M, Halmi K, Kaplan A et al. Candidate genes for anorexia nervosa in the 1p33-36 linkage region: Serotonin 1D and delta opioid receptor loci exhibit significant association to anorexia nervosa. Mol Psychiatry 2003; 8: 397-406.
16. Zhang H, Kranzler HR, Yang BZ, Luo X, Gelernter J. The OPRD1 and OPRK1 loci in alcohol or drug dependence: OPRD1 variation modulates substance dependence risk. Mol Psychiatry 2008; 13: 531-543.
17. Brown KMO, Bujac SR, Mann ET, Campbell DA, Stubbins MJ, Blundell JE. Further evidence of association of OPRD1 & HTR1D polymorphisms with susceptibility to anorexia nervosa. Biol Psychiatry 2007; 61: 367-373.
18. Knapp RJ, Malatynska E, Fang L, Li X, Babin E, Nguyen M, Santoro G, Varga EV, Hruby VJ, Roeske WR, Yamamura HI. Identification of a human delta opioid receptor: Cloning and expression. Life Sci 1994; 54: PL463-PL469.
19. Simonin F, Befort K, Gaveriaux-Ruff C, Matthes H, Nappey V, Lannes B, Micheletti G, Kieffer B. The human δ-opioid receptor: Genomic organization, cDNA cloning, functional expression, and distribution in human brain. Mol Pharmacol 1994; 46: 1015-1021.
20. Petäjä-Repo UE, Hogue M, Laperrière A, Walker P, 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 2000; 275: 13727-13736.
21. Apaja PM, Tuusa JT, Pietilä EM, Rajaniemi HJ, Petäjä-Repo UE. Luteinizing hormone receptor ectodomain splice variant misroutes the full-length receptor into a subcompartment of the endoplasmic reticulum. Mol Biol Cell 2006; 17: 2243-2255.
22. Markkanen PMH, Petäjä-Repo UE. 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 2008; 283: 29086-29098.
23. Petäjä-Repo UE, Hogue M, Bhalla S, Laperrière A, Morello JP, Bouvier M. Ligands act as pharmacological chaperones and increase the efficiency of δ opioid receptor maturation. EMBO J 2002; 21: 1628-1637.
24. LeskeläTT, Markkanen PMH, PietiläEM, Tuusa JT, Petäjä-Repo UE. Opioid receptor pharmacological chaperones act by binding and stabilizing newly synthesized receptors in the endoplasmic reticulum. J Biol Chem 2007; 282: 23171-23183.
25. Lee DH, Goldberg AL. Proteasome inhibitors: Valuable new tools for cell biologists. Trends Cell Biol 1998; 8: 397-403.
26. Petäjä-Repo UE, Hogue M, Laperrière A, Bhalla S, Walker P, 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 2001; 276: 4416-4423.
27. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007; 8: 519-529.
28. Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 2004; 11: 381-389.
29. Morello JP, Salahpour A, Laperrière A, Bernier V, Arthus MF, Lonergan M, Petäjä-Repo U, Angers S, Morin D, Bichet DG, Bouvier M. Pharmacological chaperones rescue cell-surface expression and function of misfolded V2 vasopressin receptor mutants. J Clin Invest 2000; 105: 887-895.
30. Wüller S, Wiesner B, Löffler A, Furkert J, Krause G, Hermosilla R, Schaefer M, Schülein R, Rosenthal W, Oksche A. Pharmacochaperones post-translationally enhance cell surface expression by increasing conformational stability of wild-type and mutant vasopressin V2 receptors. J Biol Chem 2004; 279: 47254-47263.
31. Schülein R, Zühlke K, Krause G, Rosenthal W. Functional rescue of the nephrogenic diabetes insipidus-causing vasopressin V2 receptor mutants G185C and R202C by a second site suppressor mutation. J Biol Chem 2001; 276: 8384-8392.
32. Saltzman AG, Morse B, Whitman MM, Ivanshchenko Y, Jaye M, Felder S. Cloning of the human serotonin 5-HT2 and 5-HT1C receptor subtypes. Biochem Biophys Res Commun 1991; 181: 1469-1478.
33. Yamada Y, Post SR, Wang K, Tager HS, Bell GI, Seino S. Cloning and functional characterization of a family of human and mouse somatostatin receptors expressed in brain, gastrointestinal tract, and kidney. Proc Natl Acad Sci U S A 1992; 89: 251-255.
34. Lappalainen J, Zhang L, Dean M, Oz M, Ozaki N, Yu DH, Virkkunen M, Weight F, Linnoila M, Goldman D. Identification, expression, and pharmacology of a Cys 23 -Ser 23 substitution in the human 5-HT 2c receptor gene (HTR2C). Genomics 1995; 27: 274-279.
35. Sanders-Bush E, Fentress H, Hazelwood L. Serotonin 5-HT 2 receptors: molecular and genomic diversity. Mol Interv 2003; 3: 319-330.
36. Fentress HM, Grinde E, Mazurkiewicz JE, Backstrom JR, Herrick-Davis K, Sanders-Bush E. Pharmacological properties of the Cys23Ser single nucleotide polymorphism in human 5-HT 2C receptor isoforms. Pharmacogenomics J 2005; 5: 244-254.
37. Rader AJ, Anderson G, Isin B, Khorana HG, Bahar I, Klein-Seetharaman J. Identification of core amino acids stabilizing rhodopsin. Proc Natl Acad Sci U S A 2004; 101: 7246-7251.
38. Anelli T, Alessio M, Bachi A, Bergamelli L, Bertoli G, Camerini S, Mezghrani A, Ruffato E, Simmen T, Sitia R. Thiol-mediated protein retention in the endoplasmic reticulum: The role of ERp44. EMBO J 2003; 22: 5015-5022.
39. Menon S, Lee J, Abplanalp WA, Yoo SE, Agui T, Furudate S, Kim PS, Arvan P. Oxidoreductase interactions include a role for ERp72 engagement with mutant thyroglobulin from the rdw/rdw rat dwarf. J Biol Chem 2007; 282: 6183-6191.
40. Ellgaard L, Ruddock LW. The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep 2005; 6: 28-32.
41. 2+ -pump SERCA2b interacts with G protein-coupled receptors and enhances their expression at the cell surface. J Mol Biol 2007; 371: 622-638.
42. Kitao Y, Imai Y, Ozawa K, Kataoka A, Ikeda T, Soda M, Nakimawa K, Kiyama H, Stern DM, Hori O, Wakamatsu K, Ito S, Itohara S, Takahashi R, Ogawa S. Pael receptor induces death of dopaminergic neurons in the substantia nigra via endoplasmic reticulum stress and dopamine toxicity, which is enhanced under condition of parkin inactivation. Hum Mol Genet 2007; 16: 50-60.
43. PietiläEM, Tuusa JT, Apaja PM, Aatsinki JT, Hakalahti AE, Rajaniemi HJ, Petäjä-Repo UE. Inefficient maturation of the rat luteinizing hormone receptor. A putative way to regulate receptor numbers at the cell surface. J Biol Chem 2005; 280: 26622-26629.
44. Petäjä-Repo UE, Hogue M, LeskeläTT, Markkanen PMH, Tuusa JT, Bouvier M. Distinct subcellular localization for constitutive and agonist-modulated palmitoylation of the human δ opioid receptor. J Biol Chem 2006; 281: 15780-15789.
45. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22: 4673-4680.
46. Schuler GD, Altschul SF, Lipman DJ. A workbench for multiple alignment construction and analysis. Proteins 1991; 9: 180-190.