Functional selectivity in serotonin receptor 2A (5-HT2A) endocytosis, recycling, and phosphorylation

Molecular Pharmacology

Volumn 83, Issue 1, 2013, Pages 42-50

  Raote, Ishier ^a   Bhattacharyya, Samarjit ^b   Panicker, Mitradas M ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH MOHALI   (India)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2,5 DIMETHOXY 4 IODOPHENYL)AMINOPROPANE; CLOZAPINE; DOPAMINE; KETANSERIN; PHOSPHOPROTEIN PHOSPHATASE 2A; PROPYLAMINE; PROTEIN KINASE C; SEROTONIN; SEROTONIN 2A RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CELL SURFACE; CHEMICAL STRUCTURE; ENDOCYTOSIS; ENZYME ACTIVATION; FUNCTIONAL GENOMICS; INTERNALIZATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

AMPHETAMINES; ANIMALS; CLOZAPINE; DOPAMINE; DRUG PARTIAL AGONISM; ENDOCYTOSIS; ENZYME ACTIVATION; HEK293 CELLS; HUMANS; KETANSERIN; LIGANDS; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN PHOSPHATASE 2; PROTEIN TRANSPORT; RATS; RECEPTOR, SEROTONIN, 5-HT2A; SEROTONIN; SEROTONIN 5-HT2 RECEPTOR AGONISTS; SEROTONIN 5-HT2 RECEPTOR ANTAGONISTS; SIGNAL TRANSDUCTION;

EID: 84871533108     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.112.078626     Document Type: Article

References (55)

1. Amanchy R, Periaswamy B, Mathivanan S, Reddy R, Tattikota SG, and Pandey A (2007) A curated compendium of phosphorylation motifs. Nat Biotechnol 25:285-286.
2. Benovic JL, DeBlasi A, Stone WC, Caron MG, and Lefkowitz RJ (1989) Beta-adrenergic receptor kinase: primary structure delineates a multigene family. Science 246:235-240. (Pubitemid 19264636)
3. Berg KA, Maayani S, Goldfarb J, Scaramellini C, Leff P, and Clarke WP (1998) Effector pathway-dependent relative efficacy at serotonin type 2A and 2C receptors: evidence for agonist-directed trafficking of receptor stimulus. Mol Pharmacol 54:94-104. (Pubitemid 28337591)
4. Berry SA, Shah MC, Khan N, and Roth BL (1996) Rapid agonist-induced internalization of the 5-hydroxytryptamine2A receptor occurs via the endosome pathway in vitro. Mol Pharmacol 50:306-313. (Pubitemid 26265135)
5. Bhatnagar A, Willins DL, Gray JA, Woods J, Benovic JL, and Roth BL (2001) The dynamin-dependent, arrestin-independent internalization of 5-hydroxytryptamine 2A (5-HT2A) serotonin receptors reveals differential sorting of arrestins and 5-HT2A receptors during endocytosis. J Biol Chem 276:8269-8277.
6. Bhattacharya A, Sankar S, and Panicker MM (2010) Differences in the C-terminus contribute to variations in trafficking between rat and human 5-HT(2A) receptor isoforms: identification of a primate-specific tripeptide ASK motif that confers GRK-2 and beta arrestin-2 interactions. J Neurochem 112:723-732.
7. Bhattacharyya S, Puri S, Miledi R, and Panicker MM (2002) Internalization and recycling of 5-HT2A receptors activated by serotonin and protein kinase C-mediated mechanisms. Proc Natl Acad Sci USA 99:14470-14475. (Pubitemid 35257695)
8. Bhattacharyya S, Raote I, Bhattacharya A, Miledi R, and Panicker MM (2006) Activation, internalization, and recycling of the serotonin 2A receptor by dopamine. Proc Natl Acad Sci USA 103:15248-15253. (Pubitemid 44583196)
9. Blaukat A, Pizard A, Breit A, Wernstedt C, Alhenc-Gelas F, Muller-Esterl W, and Dikic I (2001) Determination of bradykinin B2 receptor in vivo phosphorylation sites and their role in receptor function. J Biol Chem 276:40431-40440.
10. Blom N, Gammeltoft S, and Brunak S (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294:1351-1362. (Pubitemid 30008805)
11. Blom N, Sicheritz-Pontén T, Gupta R, Gammeltoft S, and Brunak S (2004) Prediction of post-translational glycosylation and phosphorylation of proteins from the amino acid sequence. Proteomics 4:1633-1649. (Pubitemid 38738322)
12. Calebiro D, Nikolaev VO, Gagliani MC, de Filippis T, Dees C, Tacchetti C, Persani L, and Lohse MJ (2009) Persistent cAMP-signals triggered by internalized G-protein-coupled receptors. PLoS Biol 7:e1000172.
13. Clarke WP and Bond RA (1998) The elusive nature of intrinsic efficacy. Trends Pharmacol Sci 19:270-276. (Pubitemid 28358086)
14. Gagnon AW, Kallal L, and Benovic JL (1998) Role of clathrin-mediated endocytosis in agonist-induced down-regulation of the beta2-adrenergic receptor. J Biol Chem 273:6976-6981. (Pubitemid 28160364)
15. Ghanouni P, Gryczynski Z, Steenhuis JJ, Lee TW, Farrens DL, Lakowicz JR, and Kobilka BK (2001) Functionally different agonists induce distinct conformations in the G protein coupling domain of the beta 2 adrenergic receptor. J Biol Chem 276:24433-24436.
16. González-Maeso J, Yuen T, Ebersole BJ, Wurmbach E, Lira A, Zhou M, Weisstaub N, Hen R, Gingrich JA, and Sealfon SC (2003) Transcriptome fingerprints distinguish hallucinogenic and nonhallucinogenic 5-hydroxytryptamine 2A receptor agonist effects in mouse somatosensory cortex. J Neurosci 23:8836-8843. (Pubitemid 37210895)
17. Gray JA, Sheffler DJ, Bhatnagar A, Woods JA, Hufeisen SJ, Benovic JL, and Roth BL (2001) Cell-type specific effects of endocytosis inhibitors on 5-hydroxytryptamine (2A) receptor desensitization and resensitization reveal an arrestin-, GRK2-, and GRK5-independent mode of regulation in human embryonic kidney 293 cells. Mol Pharmacol 60:1020-1030. (Pubitemid 33027437)
18. Hanley NR and Hensler JG (2002) Mechanisms of ligand-induced desensitization of the 5-hydroxytryptamine(2A) receptor. J Pharmacol Exp Ther 300:468-477.
19. Jordan BA and Devi LA (1999) G-protein-coupled receptor heterodimerization modulates receptor function. Nature 399:697-700. (Pubitemid 29289066)
20. Kalia M, Kumari S, Chadda R, Hill MM, Parton RG, and Mayor S (2006) Arf6-independent GPI-anchored protein-enriched early endosomal compartments fuse with sorting endosomes via a Rab5/phosphatidylinositol-3′-kinase- dependent machinery. Mol Biol Cell 17:3689-3704. (Pubitemid 44156459)
21. Kallal L, Gagnon AW, Penn RB, and Benovic JL (1998) Visualization of agonist-induced sequestration and down-regulation of a green fluorescent protein-tagged beta2-adrenergic receptor. J Biol Chem 273:322-328. (Pubitemid 28042212)
22. Kenakin T (2011) Functional selectivity and biased receptor signaling. J Pharmacol Exp Ther 336:296-302.
23. Ko JL, Arvidsson U, Williams FG, Law PY, Elde R, and Loh HH (1999) Visualization of time-dependent redistribution of delta-opioid receptors in neuronal cells during prolonged agonist exposure. Brain Res Mol Brain Res 69:171-185. (Pubitemid 29253810)
24. Krueger KM, Daaka Y, Pitcher JA, and Lefkowitz RJ (1997) The role of sequestration in G protein-coupled receptor resensitization. Regulation of beta2-adrenergic receptor dephosphorylation by vesicular acidification. J Biol Chem 272:5-8. (Pubitemid 27021112)
25. Law PY, Hom DS, and Loh HH (1984) Down-regulation of opiate receptor in neuroblastoma x glioma NG108-15 hybrid cells. Chloroquine promotes accumulation of tritiated enkephalin in the lysosomes. J Biol Chem 259:4096-4104. (Pubitemid 14126924)
26. Lorenz W, Inglese J, Palczewski K, Onorato JJ, Caron MG, and Lefkowitz RJ (1991) The receptor kinase family: primary structure of rhodopsin kinase reveals similarities to the beta-adrenergic receptor kinase. Proc Natl Acad Sci USA 88:8715-8719. (Pubitemid 21915427)
27. Meltzer HY, Li Z, Kaneda Y, and Ichikawa J (2003) Serotonin receptors: their key role in drugs to treat schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 27:1159-1172. (Pubitemid 37464960)
28. Meltzer HY and Massey BW (2011) The role of serotonin receptors in the action of atypical antipsychotic drugs. Curr Opin Pharmacol 11:59-67.
29. Meltzer HY, Massey BW, and Horiguchi M (2012) Serotonin receptors as targets for drugs useful to treat psychosis and cognitive impairment in schizophrenia. Curr Pharm Biotechnol 13:1572-1586.
30. Miller DD, Fleming F, Holman TL, and Perry PJ (1994) Plasma clozapine concentrations as a predictor of clinical response: a follow-up study. J Clin Psychiatry 55(Suppl B):117-121. (Pubitemid 24353033)
31. Moro O, Lameh J, and Sadée W (1993) Serine- and threonine-rich domain regulates internalization of muscarinic cholinergic receptors. J Biol Chem 268:6862-6865. (Pubitemid 23105563)
32. Nichols DE (2004) Hallucinogens. Pharmacol Ther 101:131-181. (Pubitemid 38167565)
33. Nichols DE and Nichols CD (2008) Serotonin receptors. Chem Rev 108:1614-1641. (Pubitemid 351796401)
34. Perry PJ, Miller DD, Arndt SV, and Cadoret RJ (1991) Clozapine and norclozapine plasma concentrations and clinical response of treatment-refractory schizophrenic patients. Am J Psychiatry 148:231-235.
35. Pollok-Kopp B, Schwarze K, Baradari VK, and Oppermann M (2003) Analysis of ligand-stimulated CC chemokine receptor 5 (CCR5) phosphorylation in intact cells using phosphosite-specific antibodies. J Biol Chem 278:2190-2198. (Pubitemid 36801285)
36. Potkin SG, Bera R, Gulasekaram B, Costa J, Hayes S, Jin Y, Richmond G, Carreon D, Sitanggan K, and Gerber B et al. (1994) Plasma clozapine concentrations predict clinical response in treatment-resistant schizophrenia. J Clin Psychiatry 55(Suppl B):133-136. (Pubitemid 24353037)
37. Puthenveedu MA, Lauffer B, Temkin P, Vistein R, Carlton P, Thorn K, Taunton J, Weiner OD, Parton RG, and von Zastrow M (2010) Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell 143:761-773.
38. Raote I, Bhattacharya A, and Panicker MM (2007) Serotonin 2A:5-HT2A receptor function: ligand-dependent mechanisms and pathways, in Serotonin Receptors in NeurobiologyChattopadhyay A ed.) pp 105-132, CRC Press, Boca Raton, FL.
39. Rosen H, Gonzalez-Cabrera PJ, Sanna MG, and Brown S (2009) Sphingosine 1-phosphate receptor signaling. Annu Rev Biochem 78:743-768.
40. Rozenfeld R and Devi LA (2011) Exploring a role for heteromerization in GPCR signalling specificity. Biochem J 433:11-18.
41. Sheffler DJ, Kroeze WK, Garcia BG, Deutch AY, Hufeisen SJ, Leahy P, Brüning JC, and Roth BL (2006) p90 ribosomal S6 kinase 2 exerts a tonic brake on G protein-coupled receptor signaling. Proc Natl Acad Sci USA 103: 4717-4722.
42. Sibley DR, Strasser RH, Benovic JL, Daniel K, and Lefkowitz RJ (1986) Phosphorylation/dephosphorylation of the beta-adrenergic receptor regulates its functional coupling to adenylate cyclase and subcellular distribution. Proc Natl Acad Sci USA 83:9408-9412. (Pubitemid 17223370)
43. Strachan RT, Allen JA, Sheffler DJ, and Roth BL (2010a) p90 Ribosomal S6 kinase 2, a novel GPCR kinase, is required for growth factor-mediated attenuation of GPCR signaling. Biochemistry 49:2657-2671.
44. Strachan RT, Sciaky N, Cronan MR, Kroeze WK, and Roth BL (2010b) Genetic deletion of p90 ribosomal S6 kinase 2 alters patterns of 5-hydroxytryptamine 2A serotonin receptor functional selectivity. Mol Pharmacol 77:327-338.
45. Strachan RT, Sheffler DJ, Willard B, Kinter M, Kiselar JG, and Roth BL (2009) Ribosomal S6 kinase 2 directly phosphorylates the 5-hydroxytryptamine 2A (5-HT2A) serotonin receptor, thereby modulating 5-HT2A signaling. J Biol Chem 284:5557-5573.
46. Tohgo A, Choy EW, Gesty-Palmer D, Pierce KL, Laporte S, Oakley RH, Caron MG, Lefkowitz RJ, and Luttrell LM (2003) The stability of the G protein-coupled receptor-beta-arrestin interaction determines the mechanism and functional consequence of ERK activation. J Biol Chem 278:6258-6267. (Pubitemid 36800882)
47. Tsao P, Cao T, and von Zastrow M (2001) Role of endocytosis in mediating downregulation of G-protein-coupled receptors. Trends Pharmacol Sci 22:91-96. (Pubitemid 32146487)
48. Turner JH and Raymond JR (2005) Interaction of calmodulin with the serotonin 5-hydroxytryptamine2A receptor. A putative regulator of G protein coupling and receptor phosphorylation by protein kinase C. J Biol Chem 280:30741-30750. (Pubitemid 41291803)
49. Turner JN, Coaxum SD, Gelasco AK, Garnovskaya MN, and Raymond JR (2007) Calmodulin is a 5-HT receptor-interacting and regulatory protein, in Serotonin Receptors in Neurobiology (Frontiers in Neuroscience) (Chattopadhyay A ed.) pp 61-80, CRC Press, Boca Raton, FL.
50. Urban JD, Clarke WP, and von Zastrow M et al. (2007) Functional selectivity and classical concepts of quantitative pharmacology. J Pharmacol Exp Ther 320:1-13. (Pubitemid 46025713)
51. Whistler JL (2012) Examining the role of mu opioid receptor endocytosis in the beneficial and side-effects of prolonged opioid use: from a symposium on new concepts in mu-opioid pharmacology. Drug Alcohol Depend 121:189-204.
52. Whistler JL, Chuang HH, Chu P, Jan LY, and von Zastrow M (1999) Functional dissociation of mu opioid receptor signaling and endocytosis: implications for the biology of opiate tolerance and addiction. Neuron 23:737-746. (Pubitemid 29411563)
53. Willins DL, Alsayegh L, Berry SA, Backstrom JR, Sanders-Bush E, Friedman L, Khan N, and Roth BL (1998) Serotonergic antagonist effects on trafficking of serotonin 5-HT2A receptors in vitro and in vivo. Ann N Y Acad Sci 861:121-127. (Pubitemid 29047708)
54. Willins DL, Berry SA, Alsayegh L, Backstrom JR, Sanders-Bush E, Friedman L, and Roth BL (1999) Clozapine and other 5-hydroxytryptamine-2A receptor antagonists alter the subcellular distribution of 5-hydroxytryptamine-2A receptors in vitro and in vivo. Neuroscience 91:599-606. (Pubitemid 29193269)
55. Xue Y, Li A, Wang L, Feng H, and Yao X (2006) PPSP: prediction of PK-specific phosphorylation site with Bayesian decision theory. BMC Bioinformatics 7:163.