Characterization of the 5-HT1A receptor of the honeybee (Apis mellifera) and involvement of serotonin in phototactic behavior

Cellular and Molecular Life Sciences

Volumn 67, Issue 14, 2010, Pages 2467-2479

  Thamm, Markus ^a   Balfanz, Sabine ^b   Scheiner, Ricarda ^a   Baumann, Arnd ^b   Blenau, Wolfgang ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

^b FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

5 HT; Biogenic amine; Cyclic AMP; GPCR; Phototaxis; Signal transduction

Indexed keywords

CYCLIC AMP; SEROTONIN; SEROTONIN 1A RECEPTOR; 5 CARBAMOYLTRYPTAMINE; 5-CARBOXAMIDOTRYPTAMINE; DRUG DERIVATIVE; INSECT PROTEIN; LIGAND; PRAZOSIN; SEROTONIN AGONIST; SEROTONIN ANTAGONIST;

ANIMAL BEHAVIOR; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; EMBRYO; HONEYBEE; HUMAN; HUMAN CELL; IN VIVO STUDY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; AMINO ACID SEQUENCE; ANIMAL; BEE; BRAIN; CHEMISTRY; DRUG EFFECT; GENETICS; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; LIGHT; METABOLISM; MOLECULAR GENETICS; MOVEMENT (PHYSIOLOGY); MUSHROOM BODY; OPTIC LOBE; PHYSIOLOGY;

APIS MELLIFERA; APOIDEA; DEUTEROSTOMIA; HEXAPODA; PROTOSTOMIA;

AMINO ACID SEQUENCE; ANIMALS; BEES; BEHAVIOR, ANIMAL; BRAIN; HUMANS; IMMUNOHISTOCHEMISTRY; INSECT PROTEINS; LIGANDS; LIGHT; MOLECULAR SEQUENCE DATA; MOVEMENT; MUSHROOM BODIES; OPTIC LOBE, NONMAMMALIAN; PRAZOSIN; RECEPTOR, SEROTONIN, 5-HT1A; SEROTONIN; SEROTONIN AGONISTS; SEROTONIN ANTAGONISTS;

EID: 77954593650     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-010-0350-6     Document Type: Article

References (66)

1. Weiger WA (1997) Serotonergic modulation of behaviour: a phylogenetic overview. Biol Rev Camb Philos Soc 72:61-95
2. Jones BJ, Blackburn TP (2002) The medical benefit of 5-HT research. Pharmacol Biochem Behav 71:555-568
3. Walz B, Baumann O, Krach C, Baumann A, Blenau W (2006) The aminergic control of cockroach salivary glands. Arch Insect Biochem Physiol 62:141-152
4. Colas JF, Launay JM, Kellermann O, Rosay P, Maroteaux L (1995) Drosophila 5-HT2 serotonin receptor: coexpression with fushi-tarazu during segmentation. Proc Natl Acad Sci USA 92:5441-5445
5. Yuan Q, Lin F, Zheng X, Sehgal A (2005) Serotonin modulates circadian entrainment in Drosophila. Neuron 47:115-127
6. Dierick HA, Greenspan RJ (2007) Serotonin and neuropeptide F have opposite modulatory effects on fly aggression. Nat Genet 39:678-682
7. Anstey ML, Rogers SM, Ott SR, Burrows M, Simpson SJ (2009) Serotonin mediates behavioral gregarization underlying swarm formation in desert locusts. Science 323:627-630
8. Sitaraman D, Zars M, Laferriere H, Chen YC, Sable-Smith A, Kitamoto T, Rottinghaus GE, Zars T (2008) Serotonin is necessary for place memory in Drosophila. Proc Natl Acad Sci USA 105:5579-5584
9. Taylor DJ, Robinson GE, Logan BJ, Laverty R, Mercer AR (1992) Changes in brain amine levels associated with the morphological and behavioural development of the worker honeybee. J Comp Physiol A 170:715-721
10. Wagener-Hulme C, Kuehn JC, Schulz DJ, Robinson GE (1999) Biogenic amines and division of labor in honey bee colonies. J Comp Physiol A 184:471-479
11. Schulz DJ, Robinson GE (1999) Biogenic amines and division of labor in honey bee colonies: behaviorally related changes in the antennal lobes and age-related changes in the mushroom bodies. J Comp Physiol A 184:481-488
12. Schürmann FW, Klemm N (1984) Serotonin-immunoreactive neurons in the brain of the honeybee. J Comp Neurol 225:570-580
13. Seidel C, Bicker G (1996) The developmental expression of serotonin-immunoreactivity in the brain of the pupal honeybee. Tissue Cell 28:663-672
14. Bicker G, Menzel R (1989) Chemical codes for the control of behaviour in arthropods. Nature 337:33-39
15. Menzel R, Heyne A, Kinzel C, Gerber B, Fiala A (1999) Pharmacological dissociation between the reinforcing, sensitizing, and response-releasing functions of reward in honeybee classical conditioning. Behav Neurosci 113:744-754
16. Hannon J, Hoyer D (2008) Molecular biology of 5-HT receptors. Behav Brain Res 195:198-213
17. Nichols DE, Nichols CD (2008) Serotonin receptors. Chem Rev 108:1614-1641
18. Blenau W, Baumann A (2001) Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. Arch Insect Biochem Physiol 48:13-38
19. Hauser F, Cazzamali G, Williamson M, Blenau W, Grimmelikhuijzen CJ (2006) A review of neurohormone GPCRs present in the fruitfly Drosophila melanogaster and the honey bee Apis mellifera. Prog Neurobiol 80:1-19
20. Saudou F, Boschert U, Amlaiky N, Plassat JL, Hen R (1992) A family of Drosophila serotonin receptors with distinct intracellular signalling properties and expression patterns. EMBO J 11:7-17
21. Witz P, Amlaiky N, Plassat JL, Maroteaux L, Borrelli E, Hen R (1990) Cloning and characterization of a Drosophila serotonin receptor that activates adenylate cyclase. Proc Natl Acad Sci USA 87:8940-8944
22. Blenau W, Erber J, Baumann A (1998) Characterization of a dopamine D1 receptor from Apis mellifera: cloning, functional expression, pharmacology, and mRNA localization in the brain. J Neurochem 70:15-23
23. Blenau W, Balfanz S, Baumann A (2000) Amtyr1: characterization of a gene from honeybee (Apis mellifera) brain encoding a functional tyramine receptor. J Neurochem 74:900-908
24. Grohmann L, Blenau W, Erber J, Ebert PR, Strünker T, Baumann A (2003) Molecular and functional characterization of an octopamine receptor from honeybee (Apis mellifera) brain. J Neurochem 86:725-735
25. Mustard JA, Blenau W, Hamilton IS, Ward VK, Ebert PR, Mercer AR (2003) Analysis of two D1-like dopamine receptors from the honey bee Apis mellifera reveals agonist-independent activity. Brain Res Mol Brain Res 113:67-77
26. Beggs KT, Hamilton IS, Kurshan PT, Mustard JA, Mercer AR (2005) Characterization of a D2-like dopamine receptor (Am-DOP3) in honey bee, Apis mellifera. Insect Biochem Mol Biol 35:873-882
27. Beggs KT, Mercer AR (2009) Dopamine receptor activation by honey bee queen pheromone. Curr Biol 19:1206-1209
28. Schlenstedt J, Balfanz S, Baumann A, Blenau W (2006) Am5-HT7: molecular and pharmacological characterization of the first serotonin receptor of the honeybee (Apis mellifera). J Neurochem 98:1985-1998
29. Troppmann B, Balfanz S, Baumann A, Blenau W (2010) Inverse agonist and neutral antagonist actions of synthetic compounds at an insect 5-HT1 receptor. Br J Pharmacol. doi:10.1111/j.1476-5381.2010.00638.x
30. Erber J, Hoormann J, Scheiner R (2006) Phototactic behaviour correlates with gustatory responsiveness in honey bees (Apis mellifera L.). Behav Brain Res 174:174-180
31. Käll L, Krogh A, Sonnhammer EL (2004) A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338:1027-1036
32. Moro O, Lameh J, Högger P, Sadée W (1993) Hydrophobic amino acid in the i2 loop plays a key role in receptor-G protein coupling. J Biol Chem 268:22273-22276
33. Barak LS, Tiberi M, Freedman NJ, Kwatra MM, Lefkowitz RJ, Caron MG (1994) A highly conserved tyrosine residue in G protein-coupled receptors is required for agonist-mediated b2-adrenergic receptor sequestration. J Biol Chem 269:2790-2795
34. Schäfer S, Bicker G (1986) Common projection areas of 5-HTand GABA-like immunoreactive fibers in the visual system of the honeybee. Brain Res 380:368-370
35. Ehmer B, Gronenberg W (2002) Segregation of visual input to the mushroom bodies in the honeybee (Apis mellifera). J Comp Neurol 451:362-373
36. Erber J, Kloppenburg P, Scheidler A (1993) Neuromodulation by serotonin and octopamine in the honeybee: behaviour, neuroanatomy and electrophysiology. Experientia 49:1073-1083
37. Erber J, Kloppenburg P (1995) The modulatory effects of serotonin and octopamine in the visual system of the honey bee (Apis mellifera L.). I. Behavioral analysis of the motion-sensitive antennal reflex. J Comp Physiol A 176:111-118
38. Kloppenburg P, Erber J (1995) The modulatory effects of serotonin and octopamine in the visual system of the honey bee (Apis mellifera L.). II. Electrophysiological analysis of motion-sensitive neurons in the lobula. J Comp Physiol A 176:119-129
39. Müller U (1997) Neuronal cAMP-dependent protein kinase type II is concentrated in mushroom bodies of Drosophila melanogaster and the honeybee Apis mellifera. J Neurobiol 33:33-44
40. Blenau W, Erber J (1998) Behavioural pharmacology of dopamine, serotonin and putative aminergic ligands in the mushroom bodies of the honeybee (Apis mellifera). Behav Brain Res 96:115-124
41. Kroeze WK, Kristiansen K, Roth BL (2002) Molecular biology of serotonin receptors structure and function at the molecular level. Curr Top Med Chem 2:507-528
42. Olde B, McCombie WR (1997) Molecular cloning and functional expression of a serotonin receptor from Caenorhabditis elegans. J Mol Neurosci 8:53-62
43. Barbas D, Zappulla JP, Angers S, Bouvier M, Castellucci VF, DesGroseillers L (2002) Functional characterization of a novel serotonin receptor (5-HTap2) expressed in the CNS of Aplysia californica. J Neurochem 80:335-345
44. Chen A, Holmes SP, Pietrantonio PV (2004) Molecular cloning and functional expression of a serotonin receptor from the Southern cattle tick, Boophilus microplus (Acari: Ixodidae). Insect Mol Biol 13:45-54
45. Spitzer N, Edwards DH, Baro DJ (2008) Conservation of structure, signaling and pharmacology between two serotonin receptor subtypes from decapod crustaceans, Panulirus interruptus and Procambarus clarkii. J Exp Biol 211:92-105
46. Nichols CD, Ronesi J, Pratt W, Sanders-Bush E (2002) Hallucinogens and Drosophila: linking serotonin receptor activation to behavior. Neuroscience 115:979-984
47. Johnson O, Becnel J, Nichols CD (2009) Serotonin 5-HT2 and 5-HT1A-like receptors differentially modulate aggressive behaviors in Drosophila melanogaster. Neuroscience 158:1292-1300
48. Yuan Q, Joiner WJ, Sehgal A (2006) A sleep-promoting role for the Drosophila serotonin receptor 1A. Curr Biol 16:1051-1062
49. Heisenberg M (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4:66-75
50. Giurfa M (2006) Associative learning: the instructive function of biogenic amines. Curr Biol 16:R892-R895
51. Giurfa M (2007) Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193:801-824
52. Schwärzel M, Müller U (2006) Dynamic memory networks: dissecting molecular mechanisms underlying associative memory in the temporal domain. Cell Mol Life Sci 63:989-998
53. Berry J, Krause WC, Davis RL (2008) Olfactory memory traces in Drosophila. Prog Brain Res 169:293-304
54. Mercer AR (2008) A bee-line into learning and memory mechanisms. Cell Mol Life Sci 65:3521-3524
55. Müller U (2000) Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27:159-168
56. Page RE Jr, Erber J (2002) Levels of behavioral organization and the evolution of division of labor. Naturwissenschaften 89:91-106
57. Scheiner R, Baumann A, BlenauW (2006) Aminergic control and modulation of honeybee behaviour. Curr Neuropharmacol 4:259-276
58. Mercer AR, Mobbs PG, Davenport AP, Evans PD (1983) Biogenic amines in the brain of the honeybee, Apis mellifera. Cell Tissue Res 234:655-677
59. Rodriguez Moncalvo VG, Campos AR (2009) Role of serotonergic neurons in the Drosophila larval response to light. BMC Neurosci 10:66
60. Rodríguez-Sosa L, Calderón-Rosete G, Flores G, Porras MG (2007) Serotonin-caused phase shift of circadian rhythmicity in a photosensitive neuron. Synapse 61:801-808
61. Calderón-Rosete G, Flores G, Rodríguez-Sosa L (2006) Diurnal rhythm in the levels of the serotonin 5-HT1A receptors in the crayfish eyestalk. Synapse 59:368-373
62. Claridge-Chang A, Wijnen H, Naef F, Boothroyd C, Rajewsky N, Young MW (2001) Circadian regulation of gene expression systems in the Drosophila head. Neuron 32:657-671
63. Moore D, Angel JE, Cheeseman IM, Fahrbach SE, Robinson GE (1998) Timekeeping in the honey bee colony: integration of circadian rhythms and division of labor. Behav Ecol Sociobiol 43:147-160
64. Bloch G, Robinson GE (2001) Reversal of honeybee behavioural rhythms. Nature 410:1048
65. Honeybee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931-949
66. Page RE Jr, Scheiner R, Erber J, Amdam GV (2006) The development and evolution of division of labor and foraging specialization in a social insect (Apis mellifera L.). Curr Top Dev Biol 74:253-286