Distribution of the octopamine receptor AmOA1 in the honey bee brain

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Sinakevitch, Irina ^a   Mustard, Julie A ^a   Smith, Brian H ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; OCTOPAMINE; OCTOPAMINE RECEPTOR AMOA1; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID; ANTIBODY; DIAGNOSTIC AGENT; NORSYNEPHRINE RECEPTOR; RECEPTOR;

ANATOMICAL VARIATION; ANIMAL CELL; ANIMAL TISSUE; ANTENNA (ORGAN); ARTICLE; BRAIN; CARBOXY TERMINAL SEQUENCE; CLONING; CONTROLLED STUDY; GANGLION; GENE EXPRESSION; GLOMERULUS; HONEYBEE; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; MUSHROOM BODY; NERVE FIBER; NEUROANATOMY; NEUROFEEDBACK; NEUROPIL; NONHUMAN; OLFACTORY NERVE; OPTIC LOBE; PROTEIN LOCALIZATION; ANIMAL; BEE; METABOLISM; NERVE CELL INHIBITION; PHYSIOLOGY; TISSUE DISTRIBUTION;

APIS MELLIFERA; BASIDIOMYCOTA; INVERTEBRATA;

ANIMALS; ANTIBODIES; BEES; BRAIN; GAMMA-AMINOBUTYRIC ACID; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MUSHROOM BODIES; NEURAL INHIBITION; NEUROPIL; RECEPTORS, BIOGENIC AMINE; TISSUE DISTRIBUTION;

EID: 79251549238     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014536     Document Type: Article

References (81)

1. Roeder T (1999) Octopamine in invertebrates. Prog Neurobiol 59: 533-561.
2. Verlinden H, Vleugels R, Marchal E, Badisco L, Pfluger HJ, et al. (2010) The role of octopamine in locusts and other arthropods. J Insect Physiol 56: 854-867.
3. Candy DJ (1978) The regulation of locust flight muscle metabolism by octopamine and other compounds. Insect Biochem 8: 177-181.
4. Mentel T, Duch C, Stypa H, Wegener G, Muller U, et al. (2003) Central modulatory neurons control fuel selection in flight muscle of migratory locust. J Neurosci 23: 1109-1113.
5. Davenport AP, Evans PD (1984) Stress-induced changes in the octopamine levels of insect hemolymph. Insect Biochem 14: 135-143.
6. Stern M (1999) Octopamine in the locust brain: cellular distribution and functional significance in an arousal mechanism. Microsc Res Tech 45: 135-141.
7. Wicher D (2007) Metabolic regulation and behavior: how hunger produces arousal - an insect study. Endocr Metab Immune Disord Drug Targets 7: 304-310.
8. 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.
9. Matheson T (1997) Octopamine modulates the responses and presynaptic inhibition of proprioceptive sensory neurones in the locust Schistocerca gregaria. J Exp Biol 200: 1317-1325.
10. Scheiner R, Plückhahn S, Öney B, Blenau W, Erber J (2002) Behavioural pharmacology of octopamine, tyramine and dopamine in honey bees. Behav Brain Res 136: 545-553.
11. Widmer A, Hoger U, Meisner S, French AS, Torkkeli PH (2005) Spider peripheral mechanosensory neurons are directly innervated and modulated by octopaminergic efferents. J Neurosci 25: 1588-1598.
12. Zhukovskaya MI, Kapitsky SV (2006) Activity modulation in cockroach sensillum: the role of octopamine. J Insect Physiol 52: 76-86.
13. Dierick HA (2008) Fly fighting: octopamine modulates aggression. Curr Biol 18: R161-163.
14. Hoyer SC, Eckart A, Herrel A, Zars T, Fischer SA, et al. (2008) Octopamine in male aggression of Drosophila. Curr Biol 18: 159-167.
15. Brembs B, Christiansen F, Pfluger HJ, Duch C (2007) Flight initiation and maintenance deficits in flies with genetically altered biogenic amine levels. J Neurosci 27: 11122-11131.
16. Fussnecker BL, Smith BH, Mustard JA (2006) Octopamine and tyramine influence the behavioral profile of locomotor activity in the honey bee (Apis mellifera). J Insect Physiol 52: 1083-1092.
17. Saraswati S, Fox LE, Soll DR, Wu CF (2004) Tyramine and octopamine have opposite effects on the locomotion of Drosophila larvae. J Neurobiol 58: 425-441.
18. Farooqui T, Robinson K, Vaessin H, Smith BH (2003) Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. J Neurosci 23: 5370-5380.
19. Hammer M, Menzel R (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem 5: 146-156.
20. Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, et al. (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23: 10495-10502.
21. Unoki S, Matsumoto Y, Mizunami M (2005) Participation of octopaminergic reward system and dopaminergic punishment system in insect olfactory learning revealed by pharmacological study. Eur J Neurosci 22: 1409-1416.
22. Robinson GE, Heuser LM, Le Conte Y, Lenquette F, Hollingworth RM (1999) Neurochemicals aid bee nestmate recognition. Nature 399: 534-535.
23. Spivak M, Masterman R, Ross R, Mesce KA (2003) Hygienic behavior in the honey bee (Apis mellifera L.) and the modulatory role of octopamine. J Neurobiol 55: 341-354.
24. Schulz DJ, Barron AB, Robinson GE (2002) A role for octopamine in honey bee division of labor. Brain Behav Evol 60: 350-359.
25. 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.
26. Busch S, Tanimoto H (2010) Cellular configuration of single octopamine neurons in Drosophila. J Comp Neurol 518: 2355-2364.
27. Braunig P, Burrows M, Morris OT (2004) Properties of descending dorsal unpaired median (DUM) neurons of the locust suboesophageal ganglion. Acta Biol Hung 55: 13-19.
28. Dacks AM, Christensen TA, Agricola HJ, Wollweber L, Hildebrand JG (2005) Octopamine-immunoreactive neurons in the brain and subesophageal ganglion of the hawkmoth Manduca sexta. J Comp Neurol 488: 255-268.
29. Konings PN, Vullings HG, Geffard M, Buijs RM, Diederen JH, et al. (1988) Immunocytochemical demonstration of octopamine-immunoreactive cells in the nervous system of Locusta migratoria and Schistocerca gregaria. Cell Tissue Res 251: 371-379.
30. Kreissl S, Eichmuller S, Bicker G, Rapus J, Eckert M (1994) Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. J Comp Neurol 348: 583-595.
31. Monastirioti M (1999) Biogenic amine systems in the fruit fly Drosophila melanogaster. Microsc Res Tech 45: 106-121.
32. Sinakevitch I, Niwa M, Strausfeld NJ (2005) Octopamine-like immunoreactivity in the honey bee and cockroach: comparable organization in the brain and subesophageal ganglion. J Comp Neurol 488: 233-254.
33. Sinakevitch I, Strausfeld NJ (2006) Comparison of octopamine-like immunoreactivity in the brains of the fruit fly and blow fly. J Comp Neurol 494: 460-475.
34. Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366: 59-63.
35. Schröter U, Malun D, Menzel R (2007) Innervation pattern of suboesophageal ventral unpaired median neurones in the honeybee brain. Cell Tissue Res 327: 647-667.
36. Kloppenburg P, Erber J (1995) The Modulatory Effects of serotonin and octopamine in the visual-system of the honey-bee (Apis-Mellifera L). 2. Electrophysiological analysis of motion-sensitive neurons in the lobula. J Comp Physiol A 176: 119-129.
37. 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.
38. Evans PD, Maqueira B (2005) Insect octopamine receptors: a new classification scheme based on studies of cloned Drosophila G-protein coupled receptors. Invert Neurosci 5: 111-118.
39. Balfanz S, Strunker T, Frings S, Baumann A (2005) A family of octopamine receptors that specifically induce cyclic AMP production or Ca2+ release in Drosophila melanogaster. J Neurochem 93: 440-451.
40. Han KA, Millar NS, Davis RL (1998) A novel octopamine receptor with preferential expression in Drosophila mushroom bodies. J Neurosci 18: 3650-3658.
41. Maqueira B, Chatwin H, Evans PD (2005) Identification and characterization of a novel family of Drosophila beta-adrenergic-like octopamine G-protein coupled receptors. J Neurochem 94: 547-560.
42. 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.
43. Grohmann L, Blenau W, Erber J, Ebert PR, Strunker T, et al. (2003) Molecular and functional characterization of an octopamine receptor from honeybee (Apis mellifera) brain. J Neurochem 86: 725-735.
44. Lee HG, Seong CS, Kim YC, Davis RL, Han KA (2003) Octopamine receptor OAMB is required for ovulation in Drosophila melanogaster. Dev Biol 264: 179-190.
45. Geffard M, Buijs RM, Seguela P, Pool CW, Le Moal M (1984) First demonstration of highly specific and sensitive antibodies against dopamine. Brain Res 294: 161-165.
46. Sinakevitch I, Geffard M, Pelhate M, Lapied B (1994) Octopamine-like immunoreactivity in the dorsal unpaired median (DUM) neurons innervating the accessory gland of the male cockroach Periplaneta americana. Cell & Tissue Res 276: 15-21.
47. Seguela P, Geffard M, Buijs RM, Le Moal M (1984) Antibodies against gammaaminobutyric acid: specificity studies and immunocytochemical results. Proc Natl Acad Sci U S A 81: 3888-3892.
48. Sinakevitch I, Douglass JK, Scholtz G, Loesel R, Strausfeld NJ (2003) Conserved and convergent organization in the optic lobes of insects and isopods, with reference to other crustacean taxa. J Comp Neurol 467: 150-172.
49. Sinakevitch IG, Geffard M, Pelhate M, Lapied B (1996) Anatomy and targets of Dorsal Unpaired Median neurones in the Terminal Abdominal Ganglion of the male cockroach Periplaneta americana L. J Comp Neurol 367: 147-163.
50. Brown SM, Strausfeld NJ (2006) Development-dependent and -independent ubiquitin expression in divisions of the cockroach mushroom body. J Comp Neurol 496: 556-571.
51. Sinakevitch I, Farris SM, Strausfeld NJ (2001) Taurine-, aspartate- and glutamate-like immunoreactivity identifies chemically distinct subdivisions of Kenyon cells in the cockroach mushroom body. J Comp Neurol 439: 352-367.
52. Abel R, Rybak J, Menzel R (2001) Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. J Comp Neurol 437: 363-383.
53. Flanagan D, Mercer AR (1989) An atlas and 3-D reconstruction of the antennal lobes in the worker honey bee, Apis mellifera (Hymenoptera, Apidae). Int J Insect Morph Embyrol 18: 145-159.
54. Kirschner S, Kleineidam CJ, Zube C, Rybak J, Grunewald B, et al. (2006) Dual olfactory pathway in the honeybee, Apis mellifera. J Comp Neurol 499: 933-952.
55. Arnold G, Masson C, Budharugsa S (1985) Comparative study of the antennal lobes and their afferent pathways in the worker bee and the drone (Apis mellifera). Cell Tissue Res 242: 593-605.
56. Kenyon F (1896) The brain of the bee. A preliminary contribution to the morphology of the nervous system of the Arthropoda. J Comp Neurol 6: 133-210.
57. Farris SM, Abrams AI, Strausfeld NJ (2004) Development and morphology of class II Kenyon cells in the mushroom bodies of the honey bee, Apis mellifera. J Comp Neurol 474: 325-339.
58. Mobbs P (1982) The brain of the honey bee Apis mellifera I. The connections and spatial organization of the mushrrom bodies. Philos Trans R Soc Lond B 298: 309-354.
59. Rybak J, Menzel R (1993) Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha-lobe. J Comp Neurol 334: 444-465.
60. Strausfeld NJ (2002) Organization of the honey bee mushroom body: representation of the calyx within the vertical and gamma lobes. J Comp Neurol 450: 4-33.
61. Ehmer B, Gronenberg W (2002) Segregation of visual input to the mushroom bodies in the honeybee (Apis mellifera). J Comp Neurol 451: 362-373.
62. Gronenberg W (2001) Subdivisions of hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol 435: 474-489.
63. Schröter U, Menzel R (2003) A new ascending sensory tract to the calyces of the honeybee mushroom body, the subesophageal-calycal tract. J Comp Neurol 465: 168-178.
64. Rehder V (1989) Sensory pathways and motoneurons of the proboscis reflex in the suboesophageal ganglion of the honey bee. J Comp Neurol 279: 499-513.
65. Homberg U (2008) Evolution of the central complex in the arthropod brain with respect to the visual system. Arthropod Struct Dev 37: 347-362.
66. Loesel R, Nassel DR, Strausfeld NJ (2002) Common design in a unique midline neuropil in the brains of arthropods. Arthropod Struct Dev 31: 77-91.
67. Schäfer S, Bicker G (1986) Distribution of GABA-like immunoreactivity in the brain of the honeybee. J Comp Neurol 246: 287-300.
68. Ganeshina O, Menzel R (2001) GABA-immunoreactive neurons in the mushroom bodies of the honeybee: an electron microscopic study. J Comp Neurol 437: 335-349.
69. Grünewald B (1999) Morphology of feedback neurons in the mushroom body of the honeybee, Apis mellifera. J Comp Neurol 404: 114-126.
70. Watson AH (1984) The dorsal unpaired median neurons of the locust metathoracic ganglion: neuronal structure and diversity, and synapse distribution. J Neurocytol 13: 303-327.
71. Smith BH, Wright GA, Daly KC (2006) Learning-based recognition and discrimination of floral odors. In: Dudareva N, Pichersky E, eds. The Biology and Chemistry of Floral Scents. New York: CRC Press. pp 263-295.
72. Bornhauser BC, Meyer EP (1997) Histamine-like immunoreactivity in the visual system and brain of an orthopteran and a hymenopteran insect. Cell Tissue Res 287: 211-221.
73. Yamagata N, Schmuker M, Szyszka P, Mizunami M, Menzel R (2009) Differential odor processing in two olfactory pathways in the honeybee. Front Syst Neurosci 3: 16.
74. Heimbeck G, Bugnon V, Gendre N, Keller A, Stocker RF (2001) A central neural circuit for experience-independent olfactory and courtship behavior in Drosophila melanogaster. Proc Natl Acad Sci U S A 98: 15336-15341.
75. Rybak J, Jenett A, Brandt R, Malun D (2001) Cellular localization of octopamine-like immunoreactivity in the honeybee brain. Sixth International Congress of Neuroethology; 29 July - 3 August; Bonn, Germany.
76. Bacon JP, Thompson KS, Stern M (1995) Identified octopaminergic neurons provide an arousal mechanism in the locust brain. J Neurophysiol 74: 2739-2743.
77. Rowell CHF (1971) Variable responsiveness of a visual interneurone in the freemoving locust, and its relation to behaviour and arousal. J Exp Biol 55: 727-747.
78. Rehder V (1988) A neuroanatomical map of the suboesophageal and prothoracic ganglia of the honey bee (Apis mellifera). Proc R Soc Lond B235: 179-202.
79. Strauss R (2002) The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12: 633-638.
80. Homberg U (1985) Interneurons of the central complex in the bee brain (Apis mellifera, L.). J Insect Physiol 31: 251-264.
81. Chase DL, Pepper JS, Koelle MR (2004) Mechanism of extrasynaptic dopamine signaling in Caenorhabditis elegans. Nat Neurosci 7: 1096-1103.