Protein kinase C mediates memory consolidation of taste avoidance conditioning in Lymnaea stagnalis

Neurobiology of Learning and Memory

Volumn 111, Issue , 2014, Pages 9-18

  Takigami, Satoshi ^a   Sunada, Hiroshi ^b   Lukowiak, Ken ^b   Kuzirian, Alan M ^c   Alkon, Daniel L ^d   Sakakibara, Manabu ^a  

^a TOKAI UNIVERSITY   (Japan)

^b UNIVERSITY OF CALGARY   (Canada)

^c MARINE BIOLOGICAL LABORATORY   (United States)

^d Blanchette Rockefeller Neurosciences Institute   (United States)

Author keywords

Bryostatin; Long term memory; Lymnaea stagnalis; Memory consolidation; Protein kinase C; Ro 32 0432; Short term memory; Taste avoidance conditioning

Indexed keywords

BRYOSTATIN; PROTEIN KINASE C ALPHA; PROTEIN KINASE C EPSILON; SUCROSE; PROTEIN KINASE C;

ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; CONDITIONING; CONTROLLED STUDY; DRUG EFFECT; LONG TERM MEMORY; LYMNAEA STAGNALIS; MEMORY CONSOLIDATION; NONHUMAN; SHORT TERM MEMORY; TACTILE STIMULATION; TASTE AVERSION; ANIMAL; DRUG EFFECTS; LYMNAEA; MEMORY; METABOLISM; PHYSIOLOGY; TASTE;

ANIMALS; AVOIDANCE LEARNING; BRYOSTATINS; CONDITIONING (PSYCHOLOGY); LYMNAEA; MEMORY; PROTEIN KINASE C; TASTE;

EID: 84896541080     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2014.02.011     Document Type: Article

References (60)

1. Abraham W.C., Williams J.M. LTP maintenance and its protein synthesis-dependence. Neurobiology of Learning and Memory 2008, 89:260-268.
2. Alkon D.L., Epstein H., Kuzirian A., Bennett M.C., Nelson T.J. Protein synthesis required for long-term memory is induced by PKC activation on days before associative learning. Proceedings of National Academic Science USA 2005, 102:16432-16437.
3. + channel cascade. Trends in Neurosciences 1998, 21:529-537.
4. Alkon D.L., Rasmussen H. A spatial-temporal model of cell activation. Science 1988, 239:998-1005.
5. Alkon D.L., Sun M.K., Nelson T.J. PKC signaling deficits: A mechanistic hypothesis for the origins of Alzheimer's disease. Trends in Pharmacological Sciences 2007, 28:51-60.
6. Azami S., Wagatsuma A., Sadamoto H., Hatakeyama D., Usami T., Fujie M., et al. Altered gene activity correlated with long-term memory formation of conditioned taste aversion in Lymnaea. Journal of Neuroscience Research 2006, 84:1610-1620.
7. Bank B., DeWeer A., Kuzirian A.M., Rasmussen H., Alkon D.L. Classical conditioning induces long-term translocation of protein kinase C in rabbit hippocampal CA1 cells. Proceedings of National Academic Science USA 1988, 85:1988-1992.
8. Castellucci V.F., Blumenfeld H., Goelet P., Kandel E.R. Inhibitor of protein synthesis blocks long-term behavioral sensitization in the isolated gill-withdrawal reflex of Aplysia. Journal of Neurobiology 1989, 20:1-9.
9. Crow T., Xue-Bian J.J., Siddiqi V., Kang Y., Neary J.T. Phosphorylation of mitogen-activated protein kinase by one-trial and multi-trial classical conditioning. Journal of Neuroscience 1998, 18:3480-3487.
10. Davis H.P., Squire L.R. Protein synthesis and memory: A review. Psychological Bulletin 1984, 96:518-559.
11. DeZazzo J., Tully T. Dissection of memory formation: From behavioral pharmacology to molecular genetics. Trends in Neurosciences 1995, 18:212-218.
12. Epstein H.T., Child F.M., Kuzirian A.M., Alkon D.L. Time windows for effects of protein synthesis inhibitors on Pavlovian conditioning in Hermissenda: Behavioral aspects. Neurobiology of Learning and Memory 2003, 79:127-131.
13. Epstein H.T., Kuzirian A.M., Child F.M., Alkon D.L. Two different biological configurations for long-term memory. Neurobiology of Learning and Memory 2004, 81:12-18.
14. Esposito F., Chirico G., Montesano Gesualdi N., Posadas I., Ammendola R., Russo T., et al. Protein kinase B activation by reactive oxygen species is independent of tyrosine kinase receptor phosphorylation and requires SRC activity. Journal of Biological Chemistry 2003, 278:20828-20834.
15. Farley J., Auerbach S. Protein kinase C activation induces conductance changes in Hermissenda photoreceptors like those seen in associative learning. Nature 1986, 319:220-223.
16. Fiala J.C., Spacek J., Harris K.M. Dendritic spine pathology: Cause or consequence of neurological disorders?. Brain Research. Brain Research Reviews 2002, 39:29-54.
17. Frankland P.W., Josselyn S.A. Neuroscience. Memory and the single molecule. Nature 2013, 493:312-313.
18. Fulton D., Kemenes I., Andrew R.J., Benjamin P.R. A single time-window for protein synthesis-dependent long-term memory formation after one-trial appetitive conditioning. European Journal of Neuroscience 2005, 21:1347-1358.
19. Guan Z., Kim J.H., Lomvardas S., Holick K., Xu S., Kandel E.R., et al. P38 MAP kinase mediates both short-term and long-term synaptic depression in aplysia. Journal of Neuroscience 2003, 23:7317-7325.
20. Hongpaisan J., Alkon D.L. A structural basis for enhancement of long-term associative memory in single dendritic spines regulated by PKC. Proceedings of National Academic Science USA 2007, 104:19571-19576.
21. Ito E., Kojima S., Lukowiak K., Sakakibara M. From likes to dislikes: Conditioned taste aversion in the great pond snail (Lymnaea stagnalis). Canadian Journal of Zoology 2013, 91:405-412.
22. Kawai R., Sunada H., Horikoshi T., Sakakibara M. Conditioned taste aversion with sucrose and tactile stimuli in the pond snail Lymnaea stagnalis. Neurobiology of Learning and Memory 2004, 82:164-168.
23. Kemenes I., O'Shea M., Benjamin P.R. Different circuit and monoamine mechanisms consolidate long-term memory in aversive and reward classical conditioning. European Journal of Neuroscience 2011, 33:143-152.
24. Kojima S., Yamanaka M., Fujito Y., Ito E. Differential neuroethological effects of aversive and appetitive reinforcing stimuli on associative learning in Lymnaea stagnalis. Zoological Science 1996, 13:803-812.
25. Kuzirian A.M., Epstein H.T., Gagliardi C.J., Nelson T.J., Sakakibara M., Taylor C., et al. Bryostatin enhancement of memory in Hermissenda. Biological Bulletin 2006, 210:201-214.
26. Lacchini A.H., Davies A.J., Mackintosh D., Walker A.J. Beta-1, 3-glucan modulates PKC signalling in Lymnaea stagnalis defence cells: A role for PKC in H2O2 production and downstream ERK activation. Journal of Experimental Biology 2006, 209:4829-4840.
27. Lee A.M., Kanter B.R., Wang D., Lim J.P., Zou M.E., Qiu C., et al. Prkcz null mice show normal learning and memory. Nature 2012, 493:416-419.
28. 1, a substrate for membrane protein kinase C. Brain Research 1986, 399:205-211.
29. Michel M., Kemenes I., Muller U., Kemenes G. Different phases of long-term memory require distinct temporal patterns of PKA activity after single-trial classical conditioning. Learning & Memory 2008, 15:694-702.
30. Mizumori S.J., Sakai D.H., Rosenzweig M.R., Bennett E.L., Wittreich P. Investigations into the neuropharmacological basis of temporal stages of memory formation in mice trained in an active avoidance task. Behavioural Brain Research 1987, 23:239-250.
31. Murakami J., Okada R., Sadamoto H., Kobayashi S., Mita K., Sakamoto Y., et al. Involvement of insulin-like peptide in long-term synaptic plasticity and long-term memory of the pond snail Lymnaea stagnalis. Journal of Neuroscience 2013, 33:371-383.
32. Neary J.T., Naito S., De Weer A., Alkon D.L. Ca2+/diacylglycerol-activated, phospholipid-dependent protein kinase in the Hermissenda CNS. Journal of Neurochemistry 1986, 47:1405-1411.
33. Nelson T.J., Collin C., Alkon D.L. Isolation of a G protein that is modified by learning and reduces potassium currents in Hermissenda. Science 1990, 247:1479-1483.
34. Olds J.L., Anderson M.L., McPhie D.L., Staten L.D., Alkon D.L. Imaging of memory-specific changes in the distribution of protein kinase C in the hippocampus. Science 1989, 245:866-869.
35. Ono M., Kawai R., Horikoshi T., Yasuoka T., Sakakibara M. Associative learning acquisition and retention depends on developmental stage in Lymnaea stagnalis. Neurobiology of Learning and Memory 2002, 78:53-64.
36. Pascale A., Amadio M., Scapagnini G., Lanni C., Racchi M., Provenzani A., et al. Neuronal ELAV proteins enhance mRNA stability by a PKCalpha-dependent pathway. Proceedings of National Academic Science USA 2005, 102:12065-12070.
37. Pastalkova E., Serrano P., Pinkhasova D., Wallace E., Fenton A.A., Sacktor T.C. Storage of spatial information by the maintenance mechanism of LTP. Science 2006, 313:1141-1144.
38. Quattrone A., Pascale A., Nogues X., Zhao W., Gusev P., Pacini A., et al. Posttranscriptional regulation of gene expression in learning by the neuronal ELAV-like mRNA-stabilizing proteins. Proceedings of National Academic Science USA 2001, 98:11668-11673.
39. Ramirez R.R., Gandhi C.C., Muzzio I.A., Matzel L.D. Protein synthesis-dependent memory and neuronal enhancement in Hermissenda are contingent on parameters of training and retention. Learning & Memory 1998, 4:462-477.
40. Rosenegger D., Lukowiak K. The participation of NMDA receptors, PKC, and MAPK in the formation of memory following operant conditioning in Lymnaea. Molecular Brain 2010, 3:24.
41. Rosenegger D., Lukowiak K. The participation of NMDA receptors, PKC, and MAPK in Lymnaea memory extinction. Neurobiology of Learning and Memory 2012, 100:64-69.
42. Rosenegger D., Parvez K., Lukowiak K. Enhancing memory formation by altering protein phosphorylation balance. Neurobiology of Learning and Memory 2008, 90:544-552.
43. Rosenzweig M.R., Bennett E.L., Colombo P.J., Lee D.W., Serrano P.A. Short-term, intermediate-term, and long-term memories. Behavioural Brain Research 1993, 57:193-198.
44. Sadamoto H., Sato H., Kobayashi S., Murakami J., Aonuma H., Ando H., et al. CREB in the pond snail Lymnaea stagnalis: Cloning, gene expression, and function in identifiable neurons of the central nervous system. Journal of Neurobiology 2004, 58:455-466.
45. Sandi C., Davies H.A., Cordero M.I., Rodriguez J.J., Popov V.I., Stewart M.G. Rapid reversal of stress induced loss of synapses in CA3 of rat hippocampus following water maze training. European Journal of Neuroscience 2003, 17:2447-2456.
46. Sangha S., Scheibenstock A., McComb C., Lukowiak K. Intermediate and long-term memories of associative learning are differentially affected by transcription versus translation blockers in Lymnaea. Journal of Experimental Biology 2003, 206:1605-1613.
47. Schafe G.E., LeDoux J.E. Memory consolidation of auditory pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. Journal of Neuroscience 2000, 20:RC96.
48. Shema R., Sacktor T.C., Dudai Y. Rapid erasure of long-term memory associations in the cortex by an inhibitor of PKM zeta. Science 2007, 317:951-953.
49. Smith J.B., Smith L., Pettit G.R. Bryostatins: Potent, new mitogens that mimic phorbol ester tumor promoters. Biochemical and Biophysical Research Communications 1985, 132:939-945.
50. Stough S., Shobe J.L., Carew T.J. Intermediate-term processes in memory formation. Current Opinion in Neurobiology 2006, 16:672-678.
51. Sun M.K., Alkon D.L. Synergistic effects of chronic bryostatin-1 and alpha-tocopherol on spatial learning and memory in rats. European Journal of Pharmacology 2008, 584:328-337.
52. Sutton M.A., Masters S.E., Bagnall M.W., Carew T.J. Molecular mechanisms underlying a unique intermediate phase of memory in aplysia. Neuron 2001, 31:143-154.
53. Takahashi T., Takigami S., Sunada H., Lukowiak K., Sakakibara M. Critical period of memory enhancement during taste avoidance conditioning in Lymnaea stagnalis. PLoS ONE 2013, 8:e75276.
54. Takigami S., Sunada H., Lukowiak K., Sakakibara M. High voltage with little current as an unconditional stimulus for taste avoidance conditioning in Lymnaea stagnalis. Neuroscience Letters 2013, 555:149-153.
55. Takigami S., Sunada H., Lukowiak K., Sakakibara M. Spaced taste avoidance conditioning in Lymnaea. Neurobiology of Learning and Memory 2014, 107:79-86.
56. Volk L.J., Bachman J.L., Johnson R., Yu Y., Huganir R.L. PKM-zeta is not required for hippocampal synaptic plasticity, learning and memory. Nature 2012, 493:420-423.
57. Walker T.L., Campodonico J.J., Cavallo J.S., Farley J. AA/12-lipoxygenase signaling contributes to inhibitory learning in hermissenda Type B photoreceptors. Frontiers in Behavioral Neuroscience 2010, 4.
58. Wilkinson S.E., Parker P.J., Nixon J.S. Isoenzyme specificity of bisindolylmaleimides, selective inhibitors of protein kinase C. Biochemistry Journal 1993, 294(Pt 2):335-337.
59. Wustenberg D., Gerber B., Menzel R. Short communication: Long- but not medium-term retention of olfactory memories in honeybees is impaired by actinomycin D and anisomycin. European Journal of Neuroscience 1998, 10:2742-2745.
60. Yao Y., Kelly M.T., Sajikumar S., Serrano P., Tian D., Bergold P.J., et al. PKM zeta maintains late long-term potentiation by N-ethylmaleimide-sensitive factor/GluR2-dependent trafficking of postsynaptic AMPA receptors. Journal of Neuroscience 2008, 28:7820-7827.