Induction of a specific olfactory memory leads to a long-lasting activation of protein kinase C in the antennal lobe of the honeybee

Journal of Neuroscience

Volumn 18, Issue 11, 1998, Pages 4384-4392

  Grünbaum, Lore ^a   Müller, Uli ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Antennal lobe; Memory phases; Olfactory learning; Protein kinase C; Thiol proteases; Transcription; Translation

Indexed keywords

PROTEIN KINASE C;

ANIMAL EXPERIMENT; ANTENNA; ARTICLE; CONDITIONING; ENZYME ACTIVATION; ENZYME ACTIVITY; HONEYBEE; NONHUMAN; OLFACTORY DISCRIMINATION; PRIORITY JOURNAL; RECALL; SMELLING;

EID: 0344813716     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-11-04384.1998     Document Type: Article

References (47)

1. Abel T, Nguyen PV, Barad M, Deuel AS, Kanel 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. Akers RF, Lovinger DM, Colley PA, Linden DJ, Routtenberg A (1986) Translocation of protein kinase C activity may mediate hippocampal long-term potentiation. Science 231:587-589.
3. 2+/phospholipid-dependent protein kinases in the neuronal tissue of the honeybee Apis Mellifera. Insect Biochem 21:479-486.
4. Bank B, DeWeer A, Kuzirian AM, Rasmussen H, Alkon DL (1988) Classical conditioning induces long-term translocation of protein kinase C in rabbit hippocampal CA1 cells. Proc Natl Acad Sci USA 85:1988-1992.
5. Braha O, Dale N, Hochner B, Klein M, Abrams TW, Kandel ER (1990) Second messengers involved in the two processes of facilitation in Aplysia sensory neurons. Proc Natl Acad Sci USA 87:2040-2044.
6. Bourtchouladze 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. Colley PA, Sheu F-S, Routtenberg A (1989) Dose-dependent phorbol ester facilitation or blockade of hippocampal long-term potentiation:relation to membrane/cytosol distribution of protein kinase C activity. Brain Res 495:205-216.
9. Colley PA, Sheu F-S, Routtenberg A (1990) Inhibition of protein kinase C blocks two components of LTP persistence, leaving initial potentiation intact. J Neurosci 10:3353-3360.
10. Erber J, Masuhr T, Menzel R (1980) Localization of short-term memory in the brain of the honeybee Apia mellifera. Physiol Entomol 5:343-358.
11. 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.
12. 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.
13. Golski S, Olds JL, Mishkin M, Olton DS, Alkon DL (1995) Protein kinase C in the hippocampus is altered by spatial but not cued discriminations:a component task analysis. Brain Res 676:52-62.
14. Hammer M, Menzel R (1995) Learning and memory in the honeybee. J Neurosci 15:1617-1630.
15. Hildebrandt H, Müller U (1995) Octopamine mediates rapid stimulation of protein kinase A in the antennal lobe of honeybees. J Neurobiol 27:44-50.
16. 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.
17. Kane NS, Robichon A, Dickinson JA, Greenspan RJ (1997) Learning without performance in PKC-deficient Drosophila. Neuron 18:307-314.
18. Klann E, Chen S, Sweatt JD (1991) Persistent protein kinase activation in the maintenance phase of long-term potentiation. J Biol Chem 266:24253-24256.
19. Klann E, Chen S-J, Sweatt JD (1993) Mechanism of protein kinase C activation during the induction and maintenance of long-term potentiation probed using a selective peptide substrate. Proc Natl Acad Sci USA 90:8337-8341.
20. Kleinschroth J, Hartenstein J, Rudolph C, Schächtele C (1995) Novel indolocarbazole protein kinase C inhibitors with improved biochemical and physicochemical properties. Bioorg Med Chem Lett 5:55-60.
21. Lovinger DM, Wong KL, Murakami K, Routtenberg A (1987) Protein kinase C inhibitors eliminate hippocampal long-term potentiation. Brain Res 436:177-383.
22. McPhie DL, Matzel LD, Olds JL, Lester DS, Kuzirian AM, Alkon DL (1993) Cell specificity of molecular changes during memory storage. J Neurochem 60:646-651.
23. Menzel R (1985) Learning in honeybees in an ecological and behavioral context. In:Experimental behavioral ecology (Hölldobler B, Lindauer M, eds), pp 55-74. Stuttgart, Germany:Fischer.
24. Menzel R (1990) Learning, memory and "cognition" in honeybees. In:Neurobiology of comparative cognition (Kesner RP, Olten DS, eds), pp 237-292. Hillsdale, NY:Erlbaum.
25. Menzel R, Müller U (1996) Learning and memory in honeybees:from behavior to neural substrates. Annu Rev Neurosci 19:379-404.
26. 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:Neural basis of behavioural adaptations (Schildberger K, Elsner N, eds), pp 81-102. Stuttgart, Germany:Fischer.
27. Müller U (1996) Inhibition of nitric oxide synthase impairs a distinct form of long-term memory in the honeybee, Apis mellifera. Neuron 16:541-549.
28. 2+/calmodulin and phosphorylation. Brain Res 757:24-30.
29. Müller U (1997b) 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.
30. 2+-dependent proteolytic systemcalpain-calpastatin - in the neural tissue of the honeybee Apis mellifera. Insect Biochem 21:473-477.
31. Müller U, Hildebrandt H (1995) The nitric oxide/cGMP system in the antennal lobe Apis mellifera is implicated in integrative processing of chemosensory stimuli. Eur J Neurosci 7:2240-2248.
32. Olds JL, Anderson ML, McPhie DL, Staten LD, Alkon DL (1989) Imaging of memory-specific changes in the distribution of PKC in the hippocampus. Science 245:866-869.
33. Olds JL, Golski S, McPhie DL, Olton D, Mishkin M, Alkon DL (1990) Discrimination learning alters the distribution of protein kinase C in the hippocampus of rats. J Neurosci 10:3707-3713.
34. Osten P, Valsamis L, Harris A, Sacktor TC (1996) Protein synthesís- dependent formation of protein kinase Mζ in long-term potentiation. J Neurosci 16:2444-2451.
35. Powell CM, Johnston D, Sweatt JD (1994) Autonomously active protein kinase C in the maintenance phase of N-methyl-D-aspartate receptor-independent long-term potentiation. J Biol Chem 269:27958-27963.
36. Roberson ED, Englísh JD, Sweatt JD (1996) A biochemist's view of long-term potentiation. Learn Memory 3:1-24.
37. Sacktor TC, Osten P, Valsamis H, Jiang X, Naik MU, Sublette E (1993) Persistent activation of the ζ isoform of protein kinase C in the maintenance of long-term potentiation. Proc Natl Acad Sci USA 90:8342-8346.
38. Scharenberg AM, Olds JL, Schreurs BG, Craig AM, Alkon DL (1991) PKC redistribution within CA3 stratum oriens occurring during acquisition of NM conditioning in the rabbit. Proc Natl Acad Sci USA 88:6637-6641.
39. Sossin WS, Sacktor TC, Schwartz JH (1994) Persistent activation of protein kinase C during the development of long-term facilitation in Aplysia. Learn Memory 1:189-202.
40. Sugita S, Goldsmith JR, Baxter DA, Byrne JD (1992) Involvement of protein kinase C in serotonin-induced spike broadening and synaptic facilitation in sensorimotor connections of Aplysia. J Neurophysiol 68:643-651.
41. 2+-independent form of kinase C in long-term potentiation. Biochem Biophys Res Commun 189:1514-1520.
42. Tully T, Boynton S, Brandes C, Dura JM, Mihalek R, Preat T, Villella A (1990) Genetic dissection of memory formation in Drosophila melano-gaster. Cold Spring Harbor Symp Quant Biol 55:203-211.
43. Tully T, Preat T, Boynton SC, Del Vecchio M (1994) Genetic dissection of consolidated memory in Drosophila melanogaster. Cell 79:35-47.
44. Van der Zee EA, Compaan JC, de Boer M, Luiten PGM (1992) Changes in PKCγ immunoreactivity in mouse hippocampus induced by spatial discrimination learning. J Neurosci 12:4808-4815.
45. Wang JH, Feng DP (1992) Postsynaptic protein kinase-C essential to induction and maintenance of long-term potentiation in the hippocampal CA1 region. Proc Natl Acad Sci USA 89:2576-2580.
46. 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.
47. Zhao WQ, Gibbs ME, Sedman GL, Ng KT (1994) Effect of PKC inhibitors and activators on memory. Behav Brain Res 60:151-160.