Allatostatin immunoreactivity in the honeybee brain

Journal of Comparative Neurology

Volumn 518, Issue 9, 2010, Pages 1391-1417

  Kreissl, Sabine ^a   Strasser, Christine ^a   Galizia, C Giovanni ^a  

^a UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Apis mellifera; Brain structure; Colocalization; GABA; Neuropeptides; Olfactory system

Indexed keywords

4 AMINOBUTYRIC ACID; ALLATOSTATIN;

ANTENNA; ARTICLE; BRAIN CELL; BRAIN REGION; CARBOXY TERMINAL SEQUENCE; CELL STRUCTURE; HONEYBEE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFORMATION PROCESSING; MUSHROOM BODY; NEURITE; NEUROPIL; NONHUMAN; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; OPTIC LOBE; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; VISUAL SYSTEM;

AMINO ACID SEQUENCE; ANIMALS; BEES; BRAIN; GANGLIA, INVERTEBRATE; HORMONE ANTAGONISTS; IMMUNOHISTOCHEMISTRY; MOLECULAR SEQUENCE DATA; MUSHROOM BODIES; NEURAL PATHWAYS; NEURONS; NEUROPEPTIDES;

EID: 77949411842     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22343     Document Type: Article

References (90)

1. 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.
2. Arnold G, Masson C, Budharugsa S. 1985. Comparative study of the antennal lobes and their afferent pathway in the worker bee and the drone (Apis mellifera). Cell Tissue Res 242:593-605.
3. Audsley N, Weaver RJ. 2006. Analysis of peptides in the brain and corpora cardiaca-corpora allata of the honey bee, Apis mellifera using MALDI-TOF mass spectrometry. Peptides 27:512-520.
4. Belles X, Maestro JL, Piulachs MD, Johnsen AH, Duve H, Thorpe A. 1994. Allatostatic neuropeptides from the cockroach Blattella germanica (L) (Dictyoptera, Blattellidae) - identification, immunolocalization and activity. Regul Pept 53:237-247.
5. Bendena WG, Donly BC, Tobe SS. 1999. Allatostatins: a growing family of neuropeptides with structural and functional diversity. In: Sandman CA, Strand FL, Beckwith B, Chronwall BM, Flynn FW, Nachman RJ, editors. Neuropeptides: structure and function in biology and behavior. New York: New York Academy of Sciences. p 311-329.
6. Berg BG, Schachtner J, Utz S, Homberg U. 2007. Distribution of neuropeptides in the primary olfactory center of the heliothine moth Heliothis virescens. Cell Tissue Res 327: 385-398.
7. Berg BG, Schachtner J, Homberg U. 2009. gamma-Aminobutyric acid immunostaining in the antennal lobe of the moth Heliothis virescens and its colocalization with neuropeptides. Cell Tissue Res 335:593-605.
8. Bicker G, Schäfer S, Kingan T. 1985. Mushroom body feed back interneurones in the honeybee show GABA-like immunoreactivity. Brain Res 360:394-397.
9. Bicker G, Kreissl S, Hofbauer A. 1993. Monoclonal antibody labels olfactory and visual pathways in Drosophila and Apis brains. J Comp Neurol 335:413-424.
10. Billimoria CP, DiCaprio RA, Birmingham JT, Abbott LF, Marder E. 2006. Neuromodulation of spike-timing precision in sensory neurons. J Neurosci 26:5910-5919.
11. Bloch G, Solomon SM, Robinson GE, Fahrbach SE. 2003. Patterns of PERIOD and pigment-dispersing hormone immunoreactivity in the brain of the European honeybee (Apis mellifera): age- and time-related plasticity. J Comp Neurol 464:269-284.
12. Böhm A, Neupert S, Kahnt J, Hedderich R, Predel R, Schachtner J. 2009. A mass spectrometric approach to determine neuropeptides from defined brain regions of Apis mellifera. 8th German Neurosci Conf, Göttingen. p T19-17B.
13. 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.
14. Borst A. 2009. Drosophila's view on insect vision. Curr Biol 19:R36-R47.
15. Brockmann A, Annangudi SP, Richmond TA, Ament SA, Xie F, Southey BR, Rodriguez-Zas SR, Robinson GE, Sweedler JV. 2009. Quantitative peptidomics reveal brain peptide signatures of behavior. Proc Natl Acad Sci U S A 106: 2383-2388.
16. Claeys I, Poels J, Simonet G, Franssens V, Van Loy T, Van Hiel MB, Breugelmans B, Broeck JV. 2005. Insect neuropeptide and peptide hormone receptors: current knowledge and future directions. Vitam Horm 73:217-282.
17. Davis NT, Veenstra JA, Feyereisen R, Hildebrand JG. 1997. Allatostatin-like-immunoreactive neurons of the tobacco hornworm, Manduca sexta, and isolation and identification of a new neuropeptide related to cockroach allatostatins. J Comp Neurol 385:265-284.
18. Dircksen H, Skiebe P, Abel B, Agricola H, Buchner K, Muren JE, Nässel DR. 1999. Structure, distribution, and biological activity of novel members of the allatostatin family in the crayfish Orconectes limosus. Peptides 20:695-712.
19. Duve H, Thorpe A. 1994. Distribution and functional-significance of Leu-callatostatins in the blowfly Calliphora-vomitoria. Cell Tissue Res 276:367-379.
20. Duve H, Johnsen AH, Scott AG, Yu CG, Yagi KJ, Tobe SS, Thorpe A. 1993. Callatostatins - neuropeptides from the blowfly Calliphora-vomitoria with sequence homology to cockroach allatostatins. Proc Natl Acad Sci U S A 90: 2456-2460.
21. Duve H, Wren P, Thorpe A. 1995. Innervation of the foregut of the cockroach Leucophaea-maderae and inhibition of spontaneous contractile activity by callatostatin neuropeptides. Physiol Entomol 20:33-44.
22. Duve H, Johnsen AH, Maestro JL, Scott AG, Crook N, Winstanley D, Thorpe A. 1997. Identification, tissue localisation and physiological effect in vitro of a neuroendocrine peptide identical to a dipteran Leu-callatostatin in the codling moth Cydia pomonella (Tortricidae: Lepidoptera). Cell Tissue Res 289:73-83.
23. Eichmüller S, Hammer M, Schäfer S. 1991. Neurosecretory cells in the honeybee brain and suboesophageal ganglion show FMRFamide-like immunoreactivity. J Comp Neurol 312:164-174.
24. Falkenburger BH, Barstow KL, Mintz IM. 2001. Dendrodendritic inhibition through reversal of dopamine transport. Science 293:2465-2470.
25. Fonta C, Sun XJ, Masson C. 1993. Morphology and spatial-distribution of bee antennal lobe interneurons responsive to odors. Chem Senses 18:101-119.
26. Galizia CG. 2008. Insect olfaction. In: Basbaum AIK, Shepherd GM, Westheimer G, editors. The senses: a comprehensive reference. San Diego: Academic Press. p 725-770.
27. Galizia CG, Menzel R. 2001. The role of glomeruli in the neural representation of odours: results from optical recording studies. J Insect Physiol 47:115-130.
28. Galizia CG, McIlwrath SL, Menzel R. 1999. A digital threedimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res 295:383-394.
29. Gräbner M, Groh C, Rössler W, Schachtner W. 2005. Development of allatostatin-A in antennal lobe neurons of the honeybee. In: Elsner H, editor. 6th German Neurosci Soc Conf, Göttingen: Thieme. p 832.
30. Gronenberg W. 2001. Subdivisions of hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol 435:474-489.
31. Grünewald B. 1999. Morphology of feedback neurons in the mushroom body of the honeybee, Apis mellifera. J Comp Neurol 404:114-126.
32. Hauser F, Cazzamali G, Williamson M, Blenau W, Grimmelikhuijzen CJP. 2006. A review of neurohormone GPCRs present in the fruitfly Drosophila melanogaster and the honey bee Apis mellifera. Prog Neurobiol 80:1-19.
33. Hertel H, Maronde U. 1987. The physiology and morphology of centrally projecting visual interneurons in the honeybee brain. J Exp Biol 133:301-315.
34. Hertel H, Schäfer S, Maronde U. 1987. The physiology and morphology of visual commissures in the honeybee brain. J Exp Biol 133:283-300.
35. Homberg U. 1985. Interneurones of the central complex in the bee brain (Apis mellifera, L.). J Insect Physiol 31: 251-261, 263-264.
36. Homberg U, Vitzthum H, Muller M, Binkle U. 1999. Immunocytochemistry of GABA in the central complex of the locust Schistocerca gregaria: identification of immunoreactive neurons and colocalization with neuropeptides. J Comp Neurol 409:495-507.
37. Hummon AB, Richmond TA, Verleyen P, Baggerman G, Huybrechts J, Ewing MA, Vierstraete E, Rodriguez-Zas SL, Schoofs L, Robinson GE, Sweedler JV. 2006. From the genome to the proteome: uncovering peptides in the Apis brain. Science 314:647-649.
38. Kalb J, Egelhaaf M, Kurtz R. 2008. Adaptation of velocity encoding in synaptically coupled neurons in the fly visual system. J Neurosci 28:9183-9193.
39. Katz PS. 1999. What are we talking about? Neuromodulation and its importance for information processing. In: Katz PS, editor. Beyond neurotransmission. Oxford: Oxford University Press.
40. Kirchhof BS, Homberg U, Mercer AR. 1999. Development of dopamine-immunoreactive neurons associated with the antennal lobes of the honey bee, Apis mellifera. J Comp Neurol 411:643-653.
41. Kirschner S, Kleineidam CJ, Zube C, Rybak J, Grünewald B, Rössler W. 2006. Dual olfactory pathway in the honeybee, Apis mellifera. J Comp Neurol 499:933-952.
42. Kreissl S, Eichmüller 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.
43. Kreissl S, Weiss T, Djokaj S, Balezina O, Rathmayer W. 1999. Allatostatin modulates skeletal muscle performance in crustaceans through pre- and postsynaptic effects. Eur J Neurosci 11:2519-2530.
44. Laurent G. 1996. Dynamic representation of odors by oscillating and evolving neural assemblies. Trends Neurosci 19: 489-496.
45. Maestro JL, Belles X, Piulachs MD, Thorpe A, Duve H. 1998. Localization of allatostatin-immunoreactive material in the central nervous system, stomatogastric nervous system, and gut of the cockroach Blattella germanica. Arch Insect Biochem Physiol 37:269-282.
46. Menzel R, Giurfa M. 2001. Cognitive architecture of a minibrain: the honeybee. Trends Cogn Sci 5:62-71.
47. Mobbs PG. 1982a. The brain of the honey bee Apis-mellifera 1. The connections and spatial organization of the mushroom bodies. Philos Trans R Soc Lond B Biol Sci 298:309-354.
48. Mobbs PG. 1982b. The neural architecture of the honeybee mushroom bodies. Proceedings of the International Congress of the International Union for the Study of Social Insects 9-369.
49. Mobbs PG, Kerkut GA, Gilbert LI. 1985. Brain structure. Nervous systems: structure and motor function. Oxford: Pergamon Press. p 299-370.
50. Nässel DR, Homberg U. 2006. Neuropeptides in interneurons of the insect brain. Cell Tissue Res 326:1-24.
51. Nässel DR, Enell LE, Santos JG, Wegener C, Johard HAD. 2008. A large population of diverse neurons in the Drosophila central nervous system expresses short neuropeptide F, suggesting multiple distributed peptide functions. BMC Neurosci 9:90.
52. Nishino H, Nishikawa M, Mizunami M, Yokohari F. 2009. Functional and topographic segregation of glomeruli revealed by local staining of antennal sensory neurons in the honeybee Apis mellifera. J Comp Neurol 515:161-180.
53. Pareto A. 1972. Die zentrale Verteilung der Fählerafferenzen bei Arbeiterinnen der Honigbiene, Apis mellifera. Z Zellforsch Mikrosk Anat 131:109-140.
54. Petri B, Stengl M, Wurden S, Homberg U. 1995. Immunocytochemical characterization of the accessory medulla in the cockroach Leucophaea-maderae. Cell Tissue Res 282: 3-19.
55. Predel R, Neupert S. 2007. Social behavior and the evolution of neuropeptide genes: lessons from the honeybee genome. Bioessays 29:416-421.
56. Rachinsky A, Feldlaufer MF. 2000. Responsiveness of honey bee (Apis mellifera L.) corpora allata to allatoregulatory peptides from four insect species. J Insect Physiol 46: 41-46.
57. Rehder V. 1988. A neuroanatomical map of the subesophageal and prothoracic ganglia of the honey bee (Apis-mellifera). Proc R Soc Lond Ser B Biol Sci 235:179.
58. Rehder V, Bicker G, Hammer M. 1987. Serotonin-immunoreactive neurons in the antennal lobes and suboesophageal ganglion of the honeybee. Cell Tissue Res 247:59-66.
59. Ribi WA. 1974. Neurons in the 1st synaptic region of the bee Apis-mellifera. Cell Tissue Res 148:277-286.
60. Ribi WA, Scheel M. 1981. The 2nd and 3rd optic ganglia of the worker bee Apis-mellifera Golgi studies of the neuronal elements in the medulla and lobula. Cell Tissue Res 221: 17-43.
61. 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.
62. Sachse S, Galizia CG. 2002. Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87:1106-1117.
63. Salio C, Lossi L, Ferrini F, Merighi A. 2006. Neuropeptides as synaptic transmitters. Cell Tissue Res 326:583-598.
64. Schäfer S, Bicker G. 1986. Distribution of gamma aminobutyric-acid-like immunoreactivity in the brain of the honeybee Apis-mellifera. J Comp Neurol 246:287-300.
65. Schäfer S, Rehder V. 1989. Dopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J Comp Neurol 280:43-58.
66. Schürmann FW, Erber J. 1990. FMRFamide-like immunoreactivity in the brain of the honeybee (Apis mellifera). A lightand electron microscopic study. Neuroscience 38:797-807.
67. Schürmann FW, Klemm N. 1984. Serotonin-immunoreactive neurones in the brain of the honeybee. J Comp Neurol 225:570-580.
68. 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.
69. Skiebe P, Schneider H. 1994. Allatostatin peptides in the crab stomatogastric nervous system: inhibition of the pyloric motor pattern and distribution of allatostatin-like immunoreactivity. J Exp Biol 194:195-208.
70. Stay B, Tobe SS. 2007. The role of allatostatins in juvenile hormone synthesis in insects and crustaceans. Annu Rev Entomol 52:277-299.
71. Stay B, Chan KK, Woodhead AP. 1992. Allatostatin-immunoreactive neurons projecting to the corpora allata of adult Diploptera-punctata. Cell Tissue Res 270:15-23.
72. Stay B, Tobe SS, Bendena WG. 1994. Allatostatins - identification, primary structures, functions and distribution. Adv Insect Physiol 25:267-337.
73. 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.
74. Strausfeld NJ, Homberg U, Kloppenburg P. 2000. Parallel organization in honey bee mushroom bodies by peptidergic Kenyon cells. J Comp Neurol 428:760-760.
75. Sun XJ, Fonta C, Masson C. 1993. Odor quality processing by bee antennal lobe interneurons. Chem Senses 18: 355-377.
76. Suzuki H. 1975. Antennal movements induced by odours and central projections of the antennal neurons in the honeybee. J Insect Physiol 2120:831-847.
77. Takeda K. 1961. Classical conditioned responses in the honey bee. J Insect Physiol 6:168-179.
78. Takeuchi H, Yasuda A, Yasuda-Kamatani Y, Kubo T, Nakajima T. 2003. Identification of a tachykinin-related neuropeptide from the honeybee brain using direct MALDI-TOF MS and its gene expression in worker, queen and drone heads. Insect Mol Biol 12:291-298.
79. Takeuchi H, Yasuda A, Yasuda-Kamatani Y, Sawata M, Matsuo Y, Kato A, Tsujimoto A, Nakajima T, Kubo T. 2004. Preprotachykinin gene expression in the brain of the honeybee Apis mellifera. Cell Tissue Res 316:281-293.
80. Utz S, Schachtner J. 2005. Development of A-type allatostatin immunoreactivity in antennal lobe neurons of the sphinx moth Manduca sexta. Cell Tissue Res 320:149-162.
81. Utz S, Hütteroth W, Wegener C, Kahnt J, Predel R, Schachtner J. 2007. Direct peptide profiling of lateral cell groups of the antennal lobes of Manduca sexta reveals specific composition and changes in neuropeptide expression during development. Dev Neurobiol 67:764-777.
82. Veelaert D, Schoofs L, Tobe SS, Yu CG, Vullings HGB, Couillaud F, DeLoof A. 1995a. Immunological evidence for an allatostatin-like neuropeptide in the central-nervous-system of Schistocerca-gregaria, Locusta-migratoria and Neobellieria-bullata. Cell Tissue Res 279:601-611.
83. Veelaert D, Tobe SS, Yu CG, Schoofs L, DeLoof A. 1995b. Allatostatic and allatotropic factors in the brain of the desert locust, Schistocerca-gregaria. Belg J Zool 125:243-249.
84. Veelaert D, Devreese B, Schoofs L, VanBeeumen J, Vanden-Broeck J, Tobe SS, DeLoof A. 1996. Isolation and characterization of eight myoinhibiting peptides from the desert locust, Schistocerca gregaria: new members of the cockroach allatostatin family. Mol Cell Endocrinol 122: 183-190.
85. Vitzthum H, Homberg U, Agricola H. 1996. Distribution of dipallatostatin I-like immunoreactivity in the brain of the locust Schistocerca gregaria with detailed analysis of immunostaining in the central complex. J Comp Neurol 369: 419-437.
86. Weinstock GM, Robinson GE, Gibbs RA, Worley KC, Evans JD, Maleszka R, Robertson HM, Weaver DB, Beye M, Bork P, Elsik CG, Hartfelder K, Hunt GJ, Zdobnov EM, Amdam GV, Bitondi MMG, Collins AM, Cristino AS, Lattorff HMG, Lobo CH, Moritz RFA, Nunes FMF, Page RE, Simoes ZLP, Wheeler D, Carninci P, Fukuda S, Hayashizaki Y, Kai C, Kawai J, Sakazume N, Sasaki D, Tagami M, Albert S, Baggerman G, Beggs KT, Bloch G, Cazzamali G, Cohen M, Drapeau MD, Eisenhardt D, Emore C, Ewing MA, Fahrbach SE, Foret S, Grimmelikhuijzen CJP, Hauser F, Hummon AB, Huybrechts J, Jones AK, Kadowaki T, Kaplan N, Kucharski R, Leboulle G, Linial M, Littleton JT, Mercer AR, Richmond TA, Rodriguez-Zas SL, Rubin EB, Sattelle DB, Schlipalius D, Schoofs L, Shemesh Y, Sweedler JV, Velarde R, Verleyen P, Vierstraete E, Williamson MR, Ament SA, Brown SJ, Corona M, Dearden PK, Dunn WA, Elekonich MM, Fujiyuki T, Gattermeier I, Gempe T, Hasselmann M, Kage E, Kamikouchi A, Kubo T, Kunieda T, Lorenzen M, Milshina NV, Morioka M, Ohashi K, Overbeek R, Ross CA, Schioett M, Shippy T, Takeuchi H, Toth AL, Willis JH, Wilson MJ, Gordon KHJ, Letunic I, Hackett K, Peterson J, Felsenfeld A, Guyer M, Solignac M, Agarwala R, Cornuet JM, Monnerot M, Mougel F, Reese JT, Vautrin D, Gillespie JJ, Cannone JJ, Gutell RR, Johnston JS, Eisen MB, Iyer VN, Iyer V, Kosarev P, Mackey AJ, Solovyev V, Souvorov A, Aronstein KA, Bilikova K, Chen YP, Clark AG, Decanini LI, Gelbart WM, Hetru C, Hultmark D, Imler JL, Jiang HB, Kanost M, Kimura K, Lazzaro BP, Lopez DL, Simuth J, Thompson GJ, Zou Z, De Jong P, Sodergren E, Csuros M, Milosavljevic A, Osoegawa K, Richards S, Shu CL, Duret L, Elhaik E, Graur D, Anzola JM, Campbell KS, Childs KL, Collinge D, Crosby MA, Dickens CM, Grametes LS, Grozinger CM, Jones PL, Jorda M, Ling X, Matthews BB, Miller J, Mizzen C, Peinado MA, Reid JG, Russo SM, Schroeder AJ, St Pierre SE, Wang Y, Zhou PL, Jiang HY, Kitts P, Ruef B, Venkatraman A, Zhang L, Aquino-Perez G, Whitfield CW, Behura SK, Berlocher SH, Sheppard WS, Smith DR, Suarez AV, Tsutsui ND, Wei XH, Havlak P, Li BS, Liu Y, Jolivet A, Lee S, Nazareth LV, Pu LL, Thorn R, Stolc V, Newman T, Samanta M, Tongprasit WA, Claudianos C, Berenbaum MR, Biswas S, de Graaf DC, Feyereisen R, Johnson RM, Oakeshott JG, Ranson H, Schuler MA, Muzny D, Chacko J, Davis C, Dinh H, Gill R, Hernandez J, Hines S, Hume J, Jackson L, Kovar C, Lewis L, Miner G, Morgan M, Nguyen N, Okwuonu G, Paul H, Santibanez J, Savery G, Svatek A, Villasana D, Wright R. 2006. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931-949.
87. Witthöft W. 1967. Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene. Z Morph 108:160-180.
88. Woodhead AP, Stay B, Seidel SL, Khan MA, Tobe SS. 1989. Primary structure of 4 allatostatins - neuropeptide inhibitors of juvenile-hormone synthesis. Proc Natl Acad Sci U S A 86:5997-6001.
89. Yoon JG, Stay B. 1995. Immunocytochemical localization of Diploptera punctata allatostatin-like peptide in Drosophila melanogaster. J Comp Neurol 363:475-488.
90. Zilberstein Y, Fuchs E, Hershtik L, Ayali A. 2004. Neuromodulation for behavior in the locust frontal ganglion. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 190: 301-309.