Second messenger pathways in the honeybee brain: Immunohistochemistry of protein kinase A and protein kinase C

Microscopy Research and Technique

Volumn 45, Issue 3, 1999, Pages 165-173

  Müller, Uli ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Antennal lobes; Calcium; cAMP; Learning; Memory; Mushroom bodies; Phospholipid

Indexed keywords

ANTENNA LOBES; BRAIN; CALCIUM COMPOUNDS; ENZYMES; NEURONS; PHOSPHOLIPIDS; PHOSPHORYLATION;

ANTENNAL LOBES; CA 2+; CAMP; LEARNING; MUSHROOM BODIES; NEUROPILES; OLFACTORY LEARNING; PROTEIN KINASE A; PROTEIN KINASES C; SECOND MESSENGER;

CALCIUM;

CYCLIC AMP DEPENDENT PROTEIN KINASE; PROTEIN KINASE C;

ANTENNA; ARTICLE; HONEYBEE; IMMUNOHISTOCHEMISTRY; INFORMATION PROCESSING; INSECT; LEARNING; MEMORY; NONHUMAN; OLFACTORY NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SECOND MESSENGER;

EID: 0345593714     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0029(19990501)45:3<165::AID-JEMT4>3.3.CO;2-Q     Document Type: Article

References (57)

1. Abel T, Nguyen PV, Barad M, Deuel AS, Kandel E, Bourtchouladze R. 1997. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88:615-626.
2. Altfelder K, Müller U. 1991. Cyclic nucleotide-dependent protein kinases in the neural tissue of the honeybee Apis mellifera. Insect Biochem 21:487-494.
3. 2+/Calmodulin and Ca2+/ phospholipid-dependent protein kinases in the neuronal tissue of the honeybee Apis Mellifera. Insect Biochem 21:479-486.
4. Bicker G, Menzel R. 1989. Chemical codes for the control of behavior in arthropods. Nature 337:33-39.
5. Boeckh J, Distler P, Ernst K D, Hösl M, Malun D. 1990. Olfactory bulb and antennal lobe. In: Schild D, editor. Chemosensory information processing. NATO ASI Series H39 Cell Biology. Berlin: Springer. p 201-227.
6. Bourtchuladze R, Frenguelli B, Blendy J, Cioffi D, Schutz G, Silva AJ. 1994. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79:59-68.
7. Burchuladze R, Potter J, Rose SPR. 1990. Memory formation in the chick depends on membrane-bound protein kinase C. Brain Res 535:131-138.
8. Byrne JH. 1987. Cellular analysis of associative learning. Physiol Rev 67:329-139.
9. Chao MV. 1992. Neurotrophin receptors: a window into neuronal differentiation. Neuron 9:583-593.
10. Connolly JB, Roberts IJ, Armstrong D, Kaiser K, Forte M, Tully T, O'Kane CJ. 1996. Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274:2104-2107.
11. Davis RL. 1993. Mushroom bodies and Drosophila learning. Neuron 11:1-14.
12. Davis RL, Cherry J, Dauwalder B, Han PL, Skoulakis E. 1995. The cyclic AMP system and Drosophila learning. Mol Cell Biochem 149-150:271-278.
13. deBelle JS, Heisenberg M. 1994. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263:692-695.
14. Eisenhardt D, Müller U, Kress H, Menzel R. 1997. Induction of associative olfactory memory in the honeybee: prolonged PKA activation and CREB. Soc Neurosci Abstr 23:1336.
15. Erber J, Kloppenburg P, Scheidler A. 1993. Neuromodulation by serotonin and octopamine in the honeybee: behaviour, neuroanatomy and electrophysiology. Experientia 49:1073-83.
16. Evans P. D, Robb S. 1993. Octopamine receptor subtypes and their modes of action. Neurochem Res18:869-874.
17. Farley J, Schuman E. 1991. Protein kinase C inhibitors prevent induction and continued expression of cell memory in Hermissenda type B photoreceptors. Proc Natl Acad Sci USA 88:2016-2020.
18. Fonta C, Sun XJ, Masson C. 1991. Cellular analysis of odour integration in the honeybee antennal lobe. In: Goodman LJ, Fisher RC, editors. The behaviour and physiology of bees. London: CAB International. p 227-241.
19. Frey U, Huang Y-Y, Kandel ER. 1993. Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661-1664.
20. Gascuel J, Masson C. 1991. A quantitative ultrastructural study of the honeybee antennal lobe. Tissue Cell 23:341-355.
21. Grünbaum L, Müller U. 1998. Induction of a specific olfactory memory leads to a long-lasting activation of protein kinase C in the antennal lobe of the honeybee. J Neurosci18:4384-4392.
22. Hammer M. 1993. An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59-63.
23. Hammer M. 1997. The neural basis of associative reward learning in honeybees. Trends Neurosci 20:245-252.
24. Hammer M, Menzel R. 1995. Learning and memory in the honeybee. J Neurosci 15:1617-1630.
25. Hammer M, Menzel R. 1998. Multiple sites of associative odor learning as revealed by local brain injections of octopamine in honeybees. Learn Mem 5:146-156.
26. Han JD, Baker NE, Rubin CS. 1997. Molecular characterization of a novel A kinase anchor protein from Drosophila melanogaster. J Biol Chem 272:26611-26619.
27. Han P-L, Levin LR, Reed RR, Davis RL. 1992. Preferential expression of the Drosophila rutabaga gene in mushroom bodies, neural centers for learning in insects. Neuron 9:619-627.
28. Hildebrandt H, Müller U. 1995a. Octopamine mediates rapid stimulation of PKA in the antennal lobe of honeybees. J Neurobiol 27:44-50.
29. Hildebrandt H, Müller U. 1995b. PKA activity in the antennal lobe of honeybees is regulated by chemosensory stimulation in vivo. Brain Res 679:281-288.
30. Homberg U, Christensen TA, Hildebrandt JG. 1989. Structure and function of the deutocerebrum in insects. Annu Rev Ent 34:477-501.
31. Hunter T. 1995. Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80:225-236.
32. Kaang BK, Kandel ER, Grant SG. 1993. Activation of cAMP-responsive genes by stimuli that produce long-term facilitation in Aplysia sensory neurons. Neuron 10:427-435.
33. Kalderon D, Rubin GM. 1988. Isolation and characterisation of Drosophila cAMP-dependent protein kinase genes. Genes Dev 2:1539-1556.
34. Kandel ER, Schwartz JH. 1982. Molecular biology of learning: modulation of transmitter release. Science 218:433-443.
35. Kane NS, Robichon A, Dickinson JA, Greenspan RJ. 1997. Learning without performance in PKC-deficient Drosophila. Neuron 18:307-314.
36. Kreissl S, Bicker G. 1989. Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee. J Comp Neurol 286:71-84.
37. Kreissl S, Eichmüller S, Bicker G, Rapus J, Eckert M. 1994. Octopamine-like immunoreactivity in the brain and suboesophageal ganglion of the honeybee. J Comp Neurol 348:583-595.
38. Lester LB, Scott JD. 1997. Anchoring and scaffold proteins for kinases and phosphatases. Recent Prog Horm Res 52:409-429.
39. Menzel R, Hammer M, Schneider U, Heyne M, Durst C. 1993. Aminergic modulation of associative and non-associative learning in honey bees. In: Elsner N, Heisenberg N, editors. Gene brain behaviour. Proceedings of 21th Göttingen Neurobiology Conference. Stuttgart: Thieme Verlag, p 842.
40. Menzel R, Durst C, Erber J, Eichmüller S, Hammer M, Hildebrandt H, Mauelshagen J, Müller U, Rosenboom H, Rybak J, Schäfer S, Scheidler A. 1994. The mushroom bodies in the honeybee: from molecules to behaviour. In: Schildberger K, Elsner N, editors. Neural basis of behavioural adaptations. Fortschritte der Zoologie 39. Stuttgart: Gustav Fischer Verlag. p 81-102.
41. Mercer A, Menzel R. 1982. The effects of biogenic amines on conditioned and unconditioned responses to olfactory stimuli in the honeybee Apis mellifera. J Comp Physiol 145:363-368.
42. Mercer A, Mobbs PG, Evans PD, Davenport A. 1983. Biogenic amines in the brain of the honey bee Apis mellifera. Cell Tissue Res 234:655-677.
43. 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.
44. Müller U. 1998. Signal cascades involved in olfactory learning of honeybees. Eur J Neurosci 10:261.
45. 2+-dependent proteolytic modification of the cAMP-dependent protein kinase in Drosophila wild-type and dunce memory mutants. J Neurogenet 6:95-114.
46. Newton AC. 1996. Protein kinase C: ports of anchor in the cell. Curr Biol 6:806-809.
47. Nighorn A, Healy MJ, Davis RL. 1991. The cyclic AMP phosphodiesterase encoded by the Drosophila dunce gene is concentrated in the mushroom body neuropil. Neuron 6:455-467.
48. Robb S, Cheek TR, Hannan FL, Hall LM, Midgley JM, Evans PD. 1994. Agonist-specific coupling of a cloned Drosophila octopamine/ tyramine receptor to multiple second messenger systems. EMBO J 13:1325-1330.
49. Roberson ED, English JD, Sweatt JD. 1996. A biochemist's view of long-term potentiation. Learn Mem 3:1-24.
50. Rubin CS. 1994. A kinase anchor proteins and the intracellular targeting of signals carried by cyclic AMP. Biochim Biophys Acta 1224:467-479.
51. Skoulakis EMC, Kalderon D, Davis RL. 1993. Preferential expression in mushroom bodies of the catalytic subunit of protein kinase A and its role in learning and memory. Neuron 11:197-208.
52. Sossin WS, Sacktor TC, Schwartz JH. 1994. Persistent activation of protein kinase C during the development of long-term facilitation in Aplysia. Learn Mem 1:189-202.
53. Strauss R, Heisenberg M. 1993. A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 13:1852-1861.
54. Tanaka C, Nishizuka Y. 1994. The protein kinase C family for neuronal signalling. Annu Rev Neurosci 17:551-567.
55. Taylor SS, Buechler JA, Yonemoto W. 1990. cAMP-dependent protein kinase: Framework for a diverse family of regulatory enzymes. Annu Rev Biochem 59:971-1005.
56. Yin JCP, Wallach JS, Del Vecchio M, Wilder EL, Zhou H, Quinn WG, Tully T. 1994. Induction of a dominant-negative CREB transgene specifically blocks long-term memory in Drosophila. Cell 79:49-58.
57. Zhao WQ, Gibbs ME, Sedman GL, Ng KT. 1994. Effect of PKC inhibitors and activators on memory. Behav Brain Res 60:151-160.