Targeting of the 5-HT1A serotonin receptor to neuronal dendrites is mediated by Yif1B

Journal of Neuroscience

Volumn 28, Issue 32, 2008, Pages 8063-8073

  Carrel, Damien ^a,b   Masson, Justine ^a,b   Al Awabdh, Sana ^a,b   Capra, Catherine Borg ^c   Lenkei, Zsolt ^d   Hamon, Michel ^a,b   Emerit, Michel Boris ^a,b   Darmon, Michèle ^a,b,e  

^a SORBONNE UNIVERSITÉ   (France)

^b INSERM   (France)

^c Hybrigenics SA   (France)

^d CNRS   (France)

^e PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

5 HT1A receptor; Dendrite; GPCR; Intermediate compartment; Trafficking; Yif1B

Indexed keywords

ANTIDEPRESSANT AGENT; CELL PROTEIN; COMPLEMENTARY DNA; CYAN FLUORESCENT PROTEIN; GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; RNA; SEROTONIN 1A RECEPTOR; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; YELLOW FLUORESCENT PROTEIN; YIF1B PROTEIN; NERVE PROTEIN; SEROTONIN; VESICULAR TRANSPORT PROTEIN; YIF1B PROTEIN, RAT;

ANIMAL CELL; ARTICLE; BRAIN; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITE; DRUG TARGETING; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; NERVE CELL CULTURE; NEUROMODULATION; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SEROTONINERGIC SYSTEM; TWO HYBRID SYSTEM; WESTERN BLOTTING; YEAST; ANIMAL; CELL STRAIN; CELL STRAIN COS1; CERCOPITHECUS; GENETIC TRANSFECTION; GENETICS; MALE; METABOLISM; NERVE CELL; PHYSIOLOGY; PROTEIN TRANSPORT; SPRAGUE DAWLEY RAT; SWINE; TISSUE DISTRIBUTION;

ANIMALS; BRAIN; CERCOPITHECUS AETHIOPS; COS CELLS; DENDRITES; GLUTATHIONE TRANSFERASE; LLC-PK1 CELLS; MALE; NERVE TISSUE PROTEINS; NEURONS; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, SEROTONIN, 5-HT1A; SEROTONIN; SWINE; TISSUE DISTRIBUTION; TRANSFECTION; TWO-HYBRID SYSTEM TECHNIQUES; VESICULAR TRANSPORT PROTEINS;

EID: 51149092391     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4487-07.2008     Document Type: Article

References (59)

1. Albert PR, Zhou QY, Van Tol HH, Bunzow JR, Civelli O (1990) Cloning, functional expression, and mRNA tissue distribution of the rat 5-hydroxytryptamine1A receptor gene. J Biol Chem 265:5825-5832.
2. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389-3402.
3. Alvarez VA, Ridenour DA, Sabatini BL (2006) Retraction of synapses and dendritic spines induced by off-target effects of RNA interference. J Neurosci 26:7820-7825.
4. Ango F, Robbe D, Tu JC, Xiao B, Worley PF, Pin JP, Bockaert J, Fagni L (2002) Homer-dependent cell surface expression of metabotropic glutamate receptor type 5 in neurons. Mol Cell Neurosci 20:323-329.
5. Aridor M, Guzik AK, Bielli A, Fish KN (2004) Endoplasmic reticulum export site formation and function in dendrites. J Neurosci 24:3770-3776.
6. Barnes NM, Sharp T (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38:1083-1152.
7. Barrowman J, Wang W, Zhang Y, Ferro-Novick S (2003) The Yip1p.Yif1p complex is required for the fusion competence of endoplasmic reticulum-derived vesicles. J Biol Chem 278:19878-19884.
8. Bécamel C, Alonso G, Galéotti N, Demey E, Jouin P, Ullmer C, Dumuis A, Bockaert J, Marin P (2002) Synaptic multiprotein complexes associated with 5-HT(2C) receptors: a proteomic approach. EMBO J 21:2332-2342.
9. Bécamel C, Gavarini S, Chanrion B, Alonso G, Galéotti N, Dumuis A, Bockaert J, Marin P (2004) The serotonin 5-HT2A and 5-HT2C receptors interact with specific sets of PDZ proteins. J Biol Chem 279:20257-20266.
10. Bermak JC, Li M, Bullock C, Weingarten P, Zhou QY (2002) Interaction of gamma-COP with a transport motif in the D1 receptor C-terminus. Eur J Cell Biol 81:77-85.
11. Bockaert J, Fagni L, Dumuis A, Marin P (2004) GPCR interacting proteins (GIP). Pharmacol Ther 103:203-221.
12. Boué-Grabot E, Barajas-López C, Chakfe Y, Blais D, Bélanger D, Emerit MB, Séguéla P (2003) Intracellular cross talk and physical interaction between two classes of neurotransmitter-gated channels. J Neurosci 23:1246-1253.
13. Boué-Grabot E, Emerit MB, Toulmé E, Séguéla P, Garret M (2004a) Cross-talk and co-trafficking between rho1/GABA receptors and ATP-gated channels. J Biol Chem 279:6967-6975.
14. Boué-Grabot E, Toulmé E, Emerit MB, Garret M (2004b) Subunit-specific coupling between gamma-aminobutyric acid type A and P2X2 receptor channels. J Biol Chem 279:52517-52525.
15. Brakeman PR, Lanahan AA, O'Brien R, Roche K, Barnes CA, Huganir RL, Worley PF (1997) Homer: a protein that selectively binds metabotropic glutamate receptors. Nature 386:284-288.
16. Breuza L, Halbeisen R, Jenö P, Otte S, Barlowe C, Hong W, Hauri HP (2004) Proteomics of endoplasmic reticulum-Golgi intermediate compartment (ERGIC) membranes from brefeldin A-treated HepG2 cells identifies ERGIC-32, a new cycling protein that interacts with human Erv46. J Biol Chem 279:47242-47253.
17. Brewer CB, Roth MG (1991) A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin. J Cell Biol 114:413-421.
18. Calero M, Winand NJ, Collins RN (2002) Identification of the novel proteins Yip4p and Yip5p as Rab GTPase interacting factors. FEBS Lett 515:89-98.
19. 1B serotonin receptors in plasma membrane targeting. J Cell Sci 119:4276-4284.
20. Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, Lockett S (2004) Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J 86:3993-4003.
21. 1B receptors expressed in epithelial LLC-PK1 cells. J Neurochem 71:2294-2303.
22. Doucet E, Hamon M, Emerit MB (1998) Immunolabelling of the rat intestinal tract with antibodies specific to the long form of the 5-hydroxytryptamine3 receptor. Neuroscience 87:691-707.
23. Ehret M, Pevet P, Maitre M (1991) Tryptophan hydroxylase synthesis is induced by 3′,5′-cyclic adenosine monophosphate during circadian rhythm in the rat pineal gland. J Neurochem 57:1516-1521.
24. Eimer S, Gottschalk A, Hengartner M, Horvitz HR, Richmond J, Schafer WR, Bessereau JL (2007) Regulation of nicotinic receptor trafficking by the transmembrane Golgi protein UNC-50. EMBO J 26:4313-4323.
25. el Mestikawy S, Riad M, Laporte AM, Vergé D, Daval G, Gozlan H, Hamon M (1990) Production of specific anti-rat 5-HT1A receptor antibodies in rabbits injected with a synthetic peptide. Neurosci Lett 118:189-192.
26. Filipeanu CM, Zhou F, Fugetta EK, Wu G (2006) Differential regulation of the cell-surface targeting and function of beta- and alpha1-adrenergic receptors by Rab1 GTPase in cardiac myocytes. Mol Pharmacol 69:1571-1578.
27. Formstecher E, Aresta S, Collura V, Hamburger A, Meil A, Trehin A, Reverdy C, Betin V, Maire S, Brun C, Jacq B, Arpin M, Bellaiche Y, Bellusci S, Benaroch P, Bornens M, Chanet R, Chavrier P, Delattre O, Doye V, et al. (2005) Protein interaction mapping: a Drosophila case study. Genome Res 15:376-384.
28. Gavarini S, Bécamel C, Altier C, Lory P, Poncet J, Wijnholds J, Bockaert J, Marin P (2006) Opposite effects of PSD-95 and MPP3 PDZ proteins on serotonin 5-hydroxytryptamine2C receptor desensitization and membrane stability. Mol Biol Cell 17:4619-4631.
29. Grailhe R, de Carvalho LP, Paas Y, Le Poupon C, Soudant M, Bregestovski P, Changeux JP, Corringer PJ (2004) Distinct subcellular targeting of fluorescent nicotinic alpha 3 beta 4 and serotoninergic 5-HT3A receptors in hippocampal neurons. Eur J Neurosci 19:855-862.
30. 1A autoreceptor interactions in the rat dorsal raphe nucleus: an in vitro electrophysiological study. Neuroscience 41:495-505.
31. Jasmin BJ, Cartaud J, Bornens M, Changeux JP (1989) Golgi apparatus in chick skeletal muscle: changes in its distribution during end plate development and after denervation. Proc Natl Acad Sci U S A 86:7218-7222.
32. Jin C, Zhang Y, Zhu H, Ahmed K, Fu C, Yao X (2005) Human Yip1A specifies the localization of Yif1 to the Golgi apparatus. Biochem Biophys Res Commun 334:16-22.
33. 1B receptor in axonal-apical targeting. J Neurosci 20:9111-9118.
34. 1A receptors in the rat central nervous system. J Comp Neurol 365:289-305.
35. Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567-580.
36. Kushwaha N, Harwood SC, Wilson AM, Berger M, Tecott LH, Roth BL, Albert PR (2006) Molecular determinants in the second intracellular loop of the 5-hydroxytryptamine-1A receptor for G-protein coupling. Mol Pharmacol 69:1518-1526.
37. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
38. Lanfumey L, Hamon M (2004) 5-HT1 receptors. Curr Drug Targets CNS Neurol Disord 3:1-10.
39. Lelouvier B, Tamagno G, Kaindl AM, Roland A, Lelievre V, Le Verche V, Loudes C, Gressens P, Faivre-Baumann A, Lenkei Z, Dournaud P (2008) Dynamics of somatostatin type 2A receptor cargoes in living hippocampal neurons. J Neurosci 28:4336-4349.
40. Le Poul E, Laaris N, Doucet E, Laporte AM, Hamon M, Lanfumey L (1995) Early desensitization of somato-dendritic 5-HT1A autoreceptors in rats treated with fluoxetine or paroxetine. Naunyn Schmiedebergs Arch Pharmacol 352:141-148.
41. Lim S, Naisbitt S, Yoon J, Hwang JI, Suh PG, Sheng M, Kim E (1999) Characterization of the Shank family of synaptic proteins. Multiple genes, alternative splicing, and differential expression in brain and development. J Biol Chem 274:29510-29518.
42. Matern H, Yang X, Andrulis E, Sternglanz R, Trepte HH, Gallwitz D (2000) A novel Golgi membrane protein is part of a GTPase-binding protein complex involved in vesicle targeting. EMBO J 19:4485-4492.
43. Otte S, Belden WJ, Heidtman M, Liu J, Jensen ON, Barlowe C (2001) Erv41p and Erv46p: new components of COPII vesicles involved in transport between the ER and Golgi complex. J Cell Biol 152:503-518.
44. Pierce JP, van Leyen K, McCarthy JB (2000) Translocation machinery for synthesis of integral membrane and secretory proteins in dendritic spines. Nat Neurosci 3:311-313.
45. Pierce JP, Mayer T, McCarthy JB (2001) Evidence for a satellite secretory pathway in neuronal dendritic spines. Curr Biol 11:351-355.
46. Rain JC, Selig L, De Reuse H, Battaglia V, Reverdy C, Simon S, Lenzen G, Petel F, Wojcik J, Schächter V, Chemama Y, Labigne A, Legrain P (2001) The protein-protein interaction map of Helicobacter pylori. Nature 409:211-215.
47. 1B serotonin receptors in adult rat brain. J Comp Neurol 417:181-194.
48. Sannerud R, Marie M, Nizak C, Dale HA, Pernet-Gallay K, Perez F, Goud B, Saraste J (2006) Rab1 defines a novel pathway connecting the pre-Golgi intermediate compartment with the cell periphery. Mol Biol Cell 17:1514-1526.
49. Shakoori A, Fujii G, Yoshimura S, Kitamura M, Nakayama K, Ito T, Ohno H, Nakamura N (2003) Identification of a five-pass transmembrane protein family localizing in the Golgi apparatus and the ER. Biochem Biophys Res Commun 312:850-857.
50. Sivars U, Aivazian D, Pfeffer SR (2003) Yip3 catalyses the dissociation of endosomal Rab-GDI complexes. Nature 425:856-859.
51. 1A autoreceptors on serotoninergic neurons in the midbrain raphe nuclei. Eur J Neurosci 2:1144-1154.
52. 1B receptor function by p11 in depression-like states. Science 311:77-80.
53. 1A receptor stimulates c-Jun N-terminal kinase and induces apoptosis in Chinese hamster ovary fibroblasts. Biochim Biophys Acta 1773:391-399.
54. Wojcik J, Boneca IG, Legrain P (2002) Prediction, assessment and validation of protein interaction maps in bacteria. J Mol Biol 323:763-770.
55. Wu G, Zhao G, He Y (2003) Distinct pathways for the trafficking of angiotensin II and adrenergic receptors from the endoplasmic reticulum to the cell surface: Rab1-independent transport of a G protein-coupled receptor. J Biol Chem 278:47062-47069.
56. Wyszynski M, Valtschanoff JG, Naisbitt S, Dunah AW, Kim E, Standaert DG, Weinberg R, Sheng M (1999) Association of AMPA receptors with a subset of glutamate receptor-interacting protein in vivo. J Neurosci 19:6528-6537.
57. Xia J, Zhang X, Staudinger J, Huganir RL (1999) Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron 22:179-187.
58. Yang X, Matern HT, Gallwitz D (1998) Specific binding to a novel and essential Golgi membrane protein (Yip1p) functionally links the transport GTPases Ypt1p and Ypt31p. EMBO J 17:4954-4963.
59. Ye B, Zhang Y, Song W, Younger SH, Jan LY, Jan YN (2007) Growing dendrites and axons differ in their reliance on the secretory pathway. Cell 130:717-729.