5-HT7 receptor is coupled to Gα subunits of heterotrimeric G12-protein to regulate gene transcription and neuronal morphology

Journal of Neuroscience

Volumn 25, Issue 34, 2005, Pages 7821-7830

  Kvachnina, Elena ^a   Liu, Guoquan ^b   Dityatev, Alexander ^c   Renner, Ute ^a   Dumuis, Aline ^d   Richter, Diethelm W ^a   Dityateva, Galina ^c   Schachner, Melitta ^c   Voyno Yasenetskaya, Tatyana A ^b   Ponimaskin, Evgeni G ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

Author keywords

5 HT; G protein coupled receptor; Gene transcription; Heterotrimeric G protein; Neuronal morphology; Serotonin; Small GTPases

Indexed keywords

COMPLEMENTARY DNA; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); GUANOSINE TRIPHOSPHATASE; HETEROTRIMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN CDC42; RECEPTOR SUBUNIT; RECOMBINANT DNA; SEROTONIN 4 RECEPTOR; SEROTONIN 7 RECEPTOR; SULFUR 35; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; SEROTONIN; SEROTONIN ANTAGONIST; SEROTONIN RECEPTOR;

ANIMAL CELL; ARTICLE; CELL STRAIN 3T3; CELL STRUCTURE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; FILOPODIUM; GENE EXPRESSION; GENETIC TRANSCRIPTION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE CELL; NERVE CELL CULTURE; NERVE FIBER GROWTH; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REPORTER GENE; TRANSCRIPTION REGULATION; ANIMAL; CELL CULTURE; COMPARATIVE STUDY; CYTOLOGY; DRUG ANTAGONISM; DRUG POTENTIATION; GENETICS; METABOLISM; NEURITE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; MICE; NEURITES; NEURONS; NIH 3T3 CELLS; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, SEROTONIN; SEROTONIN; SEROTONIN ANTAGONISTS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 23944516797     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1790-05.2005     Document Type: Article

References (65)

1. Aktories K, Schmidt G, Just I (2000) Rho GTPases as targets of bacterial protein toxins. Biol Chem 381:421-426.
2. Alves SE, Hoskin E, Lee SJ, Brake WG, Ferguson D, Luine V, Allen PB, Greengard P, McEwen BS (2002) Serotonin mediates CA1 spine density but is not crucial for ovarian steroid regulation of synaptic plasticity in the adult rat dorsal hippocampus. Synapse 45:143-151.
3. Amano M, Ito M, Kimura K, Fukata Y, Chihara K, Nakano T, Matsuura Y, Kaibuchi K (1996) Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J Biol Chem 271:20246-20249.
4. Azmitia EC (2001) Modern views on an ancient chemical: serotonin effects on cell proliferation, maturation, and apoptosis. Brain Res Bull 56:413-424.
5. Barnes NM, Sharp T (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38:1083-1152.
6. Buhl AM, Johnson NL, Dhanasekaran N, Johnson GL (1995) G alpha 12 and G alpha 13 stimulate Rho-dependent stress fiber formation and focal adhesion assembly. J Biol Chem 270:24631-24634.
7. Carter D, Champney M, Hwang B, Eglen RM (1995) Characterization of a postjunctional 5-HT receptor mediating relaxation of guinea-pig isolated ileum. Eur J Pharmacol 280:243-250.
8. Collins LR, Minden A, Karin M, Brown JH (1996) Galpha12 stimulates c-Jun NH2-terminal kinase through the small G proteins Ras and Rac. J Biol Chem 271:17349-17353.
9. Dityateva G, Hammond M, Thiel C, Ruonala MO, Delling M, Siebenkotten G, Nix M, Dityatev A (2003) Rapid and efficient electroporation-based gene transfer into primary dissociated neurons. J Neurosci Methods 130:65-73.
10. 1A receptors in discrete regions of the circadian timing system in hamsters. Brain Res 829:39-45.
11. Durig J, Hornung JP (2000) Neonatal serotonin depletion affects developing and mature mouse cortical neurons. NeuroReport 11:833-837.
12. Dutt P, Nguyen N, Toksoz D (2004) Role of Lbc RhoGEF in Galpha12/13-induced signals to Rho GTPase. Cell Signal 16:201-209.
13. 4 receptors. Trends Pharmacol Sci 16:391-398.
14. 2B receptor in the development of enteric neurons. J Neurosci 20:294-305.
15. Fromm C, Coso OA, Montaner S, Xu N, Gutkind JS (1997) The small GTP-binding protein Rho links G protein-coupled receptors and Galpha12 to the serum response element and to cellular transformation. Proc Natl Acad Sci USA 94:10098-10103.
16. Gonzalez GA, Montminy MR (1989) Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59:675-680.
17. Gu JL, Muller S, Mancino V, Offermanns S, Simon MI (2002) Interaction of G alpha(12) with G alpha(13) and G alpha(q) signaling pathways. Proc Natl Acad Sci USA 99:9352-9357.
18. Hagan JJ, Price GW, Jeffrey P, Deeks NJ, Stean T, Piper D, Smith MI, Upton N, Medhurst AD, Middlemiss DN, Riley GJ, Lovell PJ, Bromidge SM, Thomas DR (2000) Characterization of SB-269970-A, a selective 5-HT(7) receptor antagonist. Br J Pharmacol 130:539-548.
19. Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279:509-514.
20. Haring JH, Yan W (1999) Dentate granule cell function after neonatal treatment with parachloroamphetamine or 5,7-dihydroxytryptamine. Brain Res Dev Brain Res 114:269-272.
21. Harris TE, Persaud SJ, Jones PM (1997) Pseudosubstrate inhibition of cyclic AMP-dependent protein kinase in intact pancreatic islets: effects on cyclic AMP-dependent and glucose-dependent insulin secretion. Biochem Biophys Res Commun 232:648-651.
22. 7 receptor knockout mice. Proc Natl Acad Sci USA 100:1375-1380.
23. Hill CS, Wynne J, Treisman R (1995) The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell 81:1159-1170.
24. Igarashi M, Li WW, Sudo Y, Fishman MC (1995) Ligand-induced growth cone collapse: amplification and blockade by variant GAP-43 peptides. J Neurosci 15:5660-5667.
25. Katoh H, Aoki J, Yamaguchi Y, Kitano Y, Ichikawa A, Negishi M (1998) Constitutively active Galpha12, Galpha13, and Galphaq induce Rho-dependent neurite retraction through different signaling pathways. J Biol Chem 273:28700-28707.
26. Kawano Y, Fukata Y, Oshiro N, Amano M, Nakamura T, Ito M, Matsumura F, Inagaki M, Kaibuchi K (1999) Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo. J Cell Biol 147:1023-1038.
27. Kranenburg O, Poland M, van Horck FP, Drechsel D, Hall A, Moolenaar WH (1999) Activation of RhoA by lysophosphatidic acid and Galpha12/13 subunits in neuronal cells: induction of neurite retraction. Mol Biol Cell 10:1851-1857.
28. 7 serotonin receptor splice variants: constitutive activity and inverse agonist effects. Br J Pharmacol 135:1563-1571.
29. Lee T, Winter C, Marticke SS, Lee A, Luo L (2000) Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron 25:307-316.
30. Levitt P, Harvey JA, Friedman E, Simansky K, Murphy EH (1997) New evidence for neurotransmitter influences on brain development. Trends Neurosci 20:269-274.
31. Li Z, Van Aelst L, Cline HT (2000) Rho GTPases regulate distinct aspects of dendritic arbor growth in Xenopus central neurons in vivo. Nat Neurosci 3:217-225.
32. Li Z, Aizenman CD, Cline HT (2002) Regulation of rho GTPases by crosstalk and neuronal activity in vivo. Neuron 33:741-750.
33. Lieske V, Bennett-Clarke CA, Rhoades RW (1999) Effects of serotonin on neurite outgrowth from thalamic neurons in vitro. Neuroscience 90:967-974.
34. Liu B, Wu D (2004) Analysis of the coupling of G12/13 to G protein-coupled receptors using a luciferase reporter assay. Methods Mol Biol 237:145-149.
35. Liu JP, Lauder JM (1991) Serotonin and nialamide differentially regulate survival and growth of cultured serotonin and catecholamine neurons. Brain Res Dev Brain Res 62:297-305.
36. 7) implicated in the regulation of mammalian circadian rhythms. Neuron 11:449-458.
37. Manser E, Leung T, Salihuddin H, Zhao ZS, Lim L (1994) A brain serine/ threonine protein kinase activated by Cdc42 and Rac1. Nature 367:40-46.
38. Mao J, Yuan H, Xie W, Simon MI, Wu D (1998) Specific involvement of G proteins in regulation of serum response factor-mediated gene transcription by different receptors. J Biol Chem 273:27118-27123.
39. Meyer G, Feldman EL (2002) Signaling mechanisms that regulate actin-based motility processes in the nervous system. J Neurochem 83:490-503.
40. Neumaier JF, Sexton TJ, Yracheta J, Diaz AM, Brownfield M (2001) Localization of 5-HT(7) receptors in rat brain by immunocytochemistry, in situ hybridization, and agonist stimulated cFos expression. J Chem Neuroanat 21:63-73.
41. Ng J, Nardine T, Harms M, Tzu J, Goldstein A, Sun Y, Dietzl G, Dickson BJ, Luo L (2002) Rac GTPases control axon growth, guidance and branching. Nature 416:442-447.
42. Niu J, Profirovic J, Pan H, Vaiskunaite R, Voyno-Yasenetskaya T (2003) G Protein betagamma subunits stimulate p114RhoGEF, a guanine nucleotide exchange factor for RhoA and Rac1: regulation of cell shape and reactive oxygen species production. Circ Res 93:848-856.
43. Norrholm SD, Ouimet CC (2000) Chronic fluoxetine administration to juvenile rats prevents age-associated dendritic spine proliferation in hippocampus. Brain Res 883:205-215.
44. Offermanns S, Mancino V, Revel JP, Simon MI (1997) Vascular system defects and impaired cell chemokinesis as a result of Galpha13 deficiency. Science 275:533-536.
45. O'Kane EM, Stone TW, Morris BJ (2003) Distribution of Rho family GTPases in the adult rat hippocampus and cerebellum. Brain Res Mol Brain Res 114:1-8.
46. Olenik C, Aktories K, Meyer DK (1999) Differential expression of the small GTP-binding proteins RhoA, RhoB, Cdc42u and Cdc42b in developing rat neocortex. Brain Res Mol Brain Res 70:9-17.
47. Ponimaskin E, Harteneck C, Schultz G, Schmidt MF (1998) Acysteine-11 to serine mutant of G alpha12 impairs activation through the thrombin receptor. FEBS Lett 429:370-374.
48. Ponimaskin EG, Profirovic J, Vaiskunaite R, Richter DW, Voyno-Yasenetskaya TA (2002) 5-Hydroxytryptamine 4(a) receptor is coupled to the Galpha subunit of heterotrimeric G13 protein. J Biol Chem 277:20812-20819.
49. Prasad MV, Dermott JM, Heasley LE, Johnson GL, Dhanasekaran N (1995) Activation of Jun kinase/stress-activated protein kinase by GTPase-deficient mutants of G alpha 12 and G alpha 13. J Biol Chem 270:18655-18659.
50. Ruchhoeft ML, Ohnuma S, McNeill L, Holt CE, Harris WA (1999) The neuronal architecture of Xenopus retinal ganglion cells is sculpted by rho-family GTPases in vivo. J Neurosci 19:8454-8463.
51. Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual, Ed 2. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
52. Sebok A, Nusser N, Debreceni B, Guo Z, Santos MF, Szeberenyi J, Tigyi G (1999) Different roles for RhoA during neurite initiation, elongation, and regeneration in PC12 cells. J Neurochem 73:949-960.
53. Shen Y, Monsma Jr FJ, Metcalf MA, Jose PA, Hamblin MW, Sibley DR (1993) Molecular cloning and expression of a 5-hydroxytryptamine7 serotonin receptor subtype. J Biol Chem 268:18200-18204.
54. Stanwood GD, Washington RA, Levitt P (2001) Identification of a sensitive period of prenatal cocaine exposure that alters the development of the anterior cingulate cortex. Cereb Cortex 11:430-440.
55. Strathmann MP, Simon MI (1991) G alpha 12 and G alpha 13 subunits define a fourth class of G protein alpha subunits. Proc Natl Acad Sci USA 88:5582-5586.
56. Thomas DR, Melotto S, Massagrande M, Gribble AD, Jeffrey P, Stevens AJ, Deeks NJ, Eddershaw PJ, Fenwick SH, Riley G, Stean T, Scott CM, Hill MJ, Middlemiss DN, Hagan JJ, Price GW, Forbes IT (2003) SB-656104-A, a novel selective 5-HT7 receptor antagonist, modulates REM sleep in rats. Br J Pharmacol 139:705-714.
57. van Kesteren RE, Spencer GE (2003) The role of neurotransmitters in neurite outgrowth and synapse formation. Rev Neurosci 14:217-231.
58. 7 receptors: current knowledge and future prospects. Trends Pharmacol Sci 21:70-77.
59. Veit M, Nurnberg B, Spicher K, Harteneck C, Ponimaskin E, Schultz G, Schmidt MF (1994) The alpha-subunits of G-proteins G12 and G13 are palmitoylated, but not amidically myristoylated. FEBS Lett 339:160-164.
60. Voyno-Yasenetskaya TA, Pace AM, Bourne HR (1994) Mutant alpha subunits of G12 and G13 proteins induce neoplastic transformation of Rat-1 fibroblasts. Oncogene 9:2559-2565.
61. Wong YH, Federman A, Pace AM, Zachary I, Evans T, Pouyssegur J, Bourne HR (1991) Mutant alpha subunits of Gi2 inhibit cyclic AMP accumulation. Nature 351:63-65.
62. Xu N, Voyno-Yasenetskaya T, Gutkind JS (1994) Potent transforming activity of the G13 alpha subunit defines a novel family of oncogenes. Biochem Biophys Res Commun 201:603-609.
63. Yamamoto K, Tanimoto T, Kim S, Kikuchi A, Takai Y (1989) Small molecular weight GTP-binding proteins and signal transduction. Clin Chim Acta 185:347-355.
64. 1a receptors mediate the neurotrophic effect of serotonin on developing dentate granule cells. Brain Res Dev Brain Res 98:185-190.
65. Zipkin ID, Kindt RM, Kenyon CJ (1997) Role of a new Rho family member in cell migration and axon guidance in C. elegans. Cell 90:883-894.