Interaction of the μ-opioid receptor with synaptophysin influences receptor trafficking and signaling

Molecular Pharmacology

Volumn 71, Issue 1, 2007, Pages 123-131

  Liang, Ying Jian ^a   Wu, Dai Fei ^a   Yang, Li Quan ^a   Höllt, Volker ^a   Koch, Thomas ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIN; MU OPIATE RECEPTOR; OPIATE RECEPTOR; SYNAPTOPHYSIN;

ARTICLE; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; CELL MEMBRANE; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

BASE SEQUENCE; CELL LINE; CHROMATOGRAPHY, AFFINITY; CLONING, MOLECULAR; DNA PRIMERS; DOWN-REGULATION; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; HUMANS; KIDNEY; KINETICS; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; RADIOLIGAND ASSAY; RECEPTORS, OPIOID, MU; RECOMBINANT PROTEINS; RESTRICTION MAPPING; SIGNAL TRANSDUCTION; SYNAPTOPHYSIN;

EID: 33845913776     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.106.026062     Document Type: Article

References (42)

1. Bockaert J, Fagni L, Dumuis A, and Marin P (2004) GPCR interacting proteins (GIP). Pharmacol Ther 103:203-221.
2. Bohn LM, Gainetdinov RR, Lin FT, Lefkowitz RJ, and Caron MG (2000) Mu-opioid receptor desensitization by beta-arrestin-2 determines morphine tolerance but not dependence. Nature (Lond) 408:720-723.
3. Cameron PL, Sudhof TC, Jahn R, and De Camilli P (1991) Colocalization of synaptophysin with transferrin receptors: implications for synaptic vesicle biogenesis. J Cell Biol 115:151-164.
4. Claing A, Laporte SA, Caron MG, and Lefkowitz RJ (2002) Endocytosis of G protein-coupled receptors: roles of G protein-coupled receptor kinases and beta-arrestin proteins. Prog Neurobiol 66:61-79.
5. Daly C, Sugimori M, Moreira JE, Ziff EB, and Llinas R (2000) Synaptophysin regulates clathrin-independent endocytosis of synaptic vesicles. Proc Natl Acad Sci USA 97:6120-6125.
6. 2+-dependent formation of a dynamin-synaptophysin complex: potential role in synaptic vesicle endocytosis. J Biol Chem 277:9010-9015.
7. Evans GJ and Cousin MA (2005) Tyrosine phosphorylation of synaptophysin in synaptic vesicle recycling. Biochem Soc Trans 33:1350-1353.
8. Feng GJ, Kellett E, Scorer CA, Wilde J, White JH, and Milligan G (2003) Selective interactions between helix VIII of the human μ-opioid receptors and the C terminus of periplakin disrupt G protein activation. J Biol Chem 278:33400-33407.
9. Ferguson SS, Zhang J, Barak LS, and Caron MG (1998) Molecular mechanisms of G protein-coupled receptor desensitization and resensitization. Life Sci 62:1561-1565.
10. Finn AK and Whistler JL (2001) Endocytosis of the mu opioid receptor reduces tolerance and a cellular hallmark of opiate withdrawal. Neuron 32:829-839.
11. He L, Fong J, von Zastrow M, and Whistler JL (2002) Regulation of opioid receptor trafficking and morphine tolerance by receptor oligomerization. Cell 108:271-282.
12. Hinshaw JE (2000) Dynamin and its role in membrane fission. Annu Rev Cell Dev Biol 16:483-519.
13. Horikawa HP, Kneussel M, El Far O, and Betz H (2002) Interaction of synaptophysin with the AP-1 adaptor protein gamma-adaptin. Mol Cell Neurosci 21:454-462.
14. Keith DE, Anton B, Murray SR, Zaki PA, Chu PC, Lissin DV, Monteillet-Agius G, Stewart PL, Evans CJ, and von Zastrow M (1998) μ-Opioid receptor internalization: opiate drugs have differential effects on a conserved endocytic mechanism in vitro and in the mammalian brain. Mol Pharmacol 53:377-384.
15. Kieffer BL and Gaveriaux-Ruff C (2002) Exploring the opioid system by gene knockout. Prog Neurobiol 66:285-306.
16. 2 modulates agonist-induced mu-opioid receptor desensitization and resensitization. J Neurochem 88:680-688.
17. Koch T, Brandenburg LO, Schulz S, Liang Y, Klein J, and Höllt V (2003) ADPribosylation factor-dependent phospholipase D2 activation is required for agonist-induced μ-opioid receptor endocytosis. J Biol Chem 278:9979-9985.
18. Koch T, Schulz S, Schröder H, Wolf R, Raulf E, and Höllt V (1998) Carboxyl-terminal splicing of the rat μ opioid receptor modulates agonist-mediated internalization and receptor resensitization. J Biol Chem 273:13652-13657.
19. Koch T, Widera A, Bartzsch K, Schulz S, Brandenburg LO, Wundrack N, Beyer A, Grecksch G, and Höllt V (2005) Receptor endocytosis counteracts the development of opioid tolerance. Mol Pharmacol 67:280-287.
20. Koch T, Wu DF, Yang LQ, Brandenburg LO, and Höllt V (2006) Role of phospholipase D2 in the agonist-induced and constitutive endocytosis of G-protein couple receptors. J Neurochem 97:365-372.
21. Law PY, Erickson LJ, El-Kouhen R, Dicker L, Solberg J, Wang W, Miller E, Burd AL, and Loh HH (2000) Receptor density and recycling affect the rate of agonist-induced desensitization of μ-opioid receptor. Mol Pharmacol 58:388-398.
22. Lefkowitz RJ, Pitcher J, Krueger K, and Daaka Y (1998) Mechanisms of beta-adrenergic receptor desensitization and resensitization. Adv Pharmacol 42:416-420.
23. Leterrier C, Laine J, Darmon M, Boudin H, Rossier J, and Lenkei Z (2006) Constitutive activation drives compartment-selective endocytosis and axonal targeting of type 1 cannabinoid receptors. J Neurosci 26:3141-3153.
24. Liao D, Lin H, Law PY, and Loh HH (2005) Mu-opioid receptors modulate the stability of dendritic spines. Proc Natl Acad Sci USA 102:1725-1730.
25. Linstedt AD and Kelly RB (1991) Endocytosis of the synaptic vesicle protein, synaptophysin, requires the COOH-terminal tail. J Physiol (Paris) 85:90-96.
26. Matthes HW, Maldonado R, Simonin F, Valverde O, Slowe S, Kitchen I, Befort K, Dierich A, Le Meur M, Dolle P, et al. (1996) Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature (Lond) 383:819-823.
27. Mousavi SA, Malerod L, Berg T, and Kjeken R (2004) Clathrin-dependent endocytosis. Biochem J 377:1-16.
28. Olive MF, Anton B, Micevych P, Evans CJ, and Maidment NT (1997) Presynaptic versus postsynaptic localization of mu and delta opioid receptors in dorsal and ventral striatopallidal pathways. J Neurosci 17:7471-7479.
29. Onoprishvili I, Andria ML, Kramer HK, Ancevska-Taneva N, Hiller JM, and Simon EJ (2003) Interaction between the μ opioid receptor and filamin A is involved in receptor regulation and trafficking. Mol Pharmacol 64:1092-1100.
30. Pak Y, Kouvelas A, Scheideler MA, Rasmussen J, O'Dowd BF, and George SR (1996) Agonist-induced functional desensitization of the μ-opioid receptor is mediated by loss of membrane receptors rather than uncoupling from G protein. Mol Pharmacol 50:1214-1222.
31. Pfeiffer M, Kirscht S, Stumm R, Koch T, Wu D, Laugsch M, Schröder H, Höllt V, and Schulz S (2003) Heterodimerization of substance P and μ-opioid receptors regulates receptor trafficking and resensitization. J Biol Chem 278:51630-51637.
32. Pfleger KD and Eidne KA (2003) New technologies: bioluminescence resonance energy transfer (BRET) for the detection of real time interactions involving Gprotein coupled receptors. Pituitary 6:141-151.
33. Qiu Y, Law PY, and Loh HH (2003) μ-Opioid receptor desensitization: role of receptor phosphorylation, internalization, and representation. J Biol Chem 278:36733-36739.
34. Robinson MS and Bonifacino JS (2001) Adaptor-related proteins. Curr Opin Cell Biol 13:444-453.
35. Seaman MN, Sowerby PJ, and Robinson MS (1996) Cytosolic and membrane-associated proteins involved in the recruitment of AP-1 adaptors onto the Trans-Golgi network. J Biol Chem 271:25446-25451.
36. Slepnev VI, Ochoa GC, Butler MH, and De Camilli P (2000) Tandem arrangement of the clathrin and AP-2 binding domains in amphiphysin 1 and disruption of clathrin coat function by amphiphysin fragments comprising these sites. J Biol Chem 275:17583-17589.
37. Sudhof TC, Lottspeich F, Greengard P, Mehl E, and Jahn R (1987) A synaptic vesicle protein with a novel cytoplasmic domain and four transmembrane regions. Science (Wash DC) 238:1142-1144.
38. Svingos AL, Moriwaki A, Wang JB, Uhl GR, and Pickel VM (1996) Ultrastructural immunocytochemical localization of mu-opioid receptors in rat nucleus accumbens: extrasynaptic plasmalemmal distribution and association with Leu5-enkephalin. J Neurosci 16:4162-4173.
39. Thiele C, Hannah MJ, Fahrenholz F, and Huttner WB (2000) Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat Cell Biol 2:42-49.
40. Tsao PI and von Zastrow M (2000) Type-specific sorting of G protein-coupled receptors after endocytosis. J Biol Chem 275:11130-11140.
41. Valtorta F, Pennuto M, Bonanomi D, and Benfenati F (2004) Synaptophysin: leading actor or walk-on role in synaptic vesicle exocytosis? Bioessays 26:445-453.
42. Zhang J, Ferguson SS, Barak LS, Bodduluri SR, Laporte SA, Law PY, and Caron MG (1998) Role for G protein-coupled receptor kinase in agonist-specific regulation of mu-opioid receptor responsiveness. Proc Natl Acad Sci USA 95:7157-7162.