Involvement of insulin-like peptide in long-term synaptic plasticity and long-term memory of the pond snail Lymnaea stagnalis

Journal of Neuroscience

Volumn 33, Issue 1, 2013, Pages 371-383

  Murakami, Jun ^a   Okada, Ryuichi ^a   Sadamoto, Hisayo ^a   Kobayashi, Suguru ^a   Mita, Koichi ^a   Sakamoto, Yuki ^a   Yamagishi, Miki ^a   Hatakeyama, Dai ^a   Otsuka, Emi ^a   Okuta, Akiko ^b   Sunada, Hiroshi ^c   Takigami, Satoshi ^c   Sakakibara, Manabu ^c   Fujito, Yutaka ^d   Awaji, Masahiko ^e   Moriyama, Shunsuke ^f   Lukowiak, Ken ^g   Ito, Etsuro ^a  

^a TOKUSHIMA BUNRI UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c TOKAI UNIVERSITY   (Japan)

^d SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e FISHERIES RESEARCH AGENCY   (Japan)

^f KITASATO UNIVERSITY   (Japan)

^g UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN RECEPTOR ANTIBODY; MOLLUSCAN INSULIN RELATED PEPTIDE; NEUROPEPTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GEL PERMEATION CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN SITU HYBRIDIZATION; LONG TERM MEMORY; LYMNAEA STAGNALIS; MASS SPECTROMETRY; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SYNAPTIC EFFICACY; TASTE AVERSION;

ANIMALS; AVOIDANCE LEARNING; CONDITIONING, CLASSICAL; INSULIN; LYMNAEA; MEMORY, LONG-TERM; NEURONAL PLASTICITY; NEURONS; NEUROPEPTIDES; SYNAPSES; TASTE;

EID: 84871771576     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0679-12.2013     Document Type: Article

References (82)

1. Aberg D (2010) Role of the growth hormone/insulin-like growth factor 1 axis in neurogenesis. Endocr Dev 17:63-76. Medline
2. Amano H, Maruyama IN (2011) Aversive olfactory learning and associative long-term memory in Caenorhabditis elegans. Learn Mem 18:654-665. CrossRef Medline
3. Azami S, Wagatsuma A, Sadamoto H, Hatakeyama D, Usami T, Fujie M, Koyanagi R, Azumi K, Fujito Y, Lukowiak K, Ito E (2006) Altered gene activity correlated with long-term memory formation of conditioned taste aversion in Lymnaea. J Neurosci Res 84:1610-1620. CrossRef Medline
4. Benjamin PR, Rose RM, Slade CT, Lacy MG (1979) Morphology of identified neurones in the buccal ganglia of Lymnaea stagnalis. J Exp Biol 80:119-135.
5. Benjamin PR, Staras K, Kemenes G (2000) A systems approach to the cellular analysis of associative learning in the pond snail Lymnaea. Learn Mem 7:124-131. CrossRef Medline
6. Braun MH, Lukowiak K (2011) Intermediate and long-term memory are different at the neuronal level in Lymnaea stagnalis (L.). Neurobiol Learn Mem 96:403-416. CrossRef Medline
7. Chiu SL, Chen CM, Cline HT (2008) Insulin receptor signaling regulates synapse number, dendritic plasticity, and circuit function in vivo. Neuron 58:708-719. CrossRef Medline
8. Craft S, Baker LD, Montine TJ, Minoshima S, Watson GS, Claxton A, Arbuckle M, Callaghan M, Tsai E, Plymate SR, Green PS, Leverenz J, Cross D, Gerton B (2012) Intranasal insulin therapy for Alzheimer disease and amnestic mild cognitive impairment: a pilot clinical trial. Arch Neurol 69:29-38. CrossRef Medline
9. Dalesman S, Lukowiak K (2010) Effect of acute exposure to low environmental calcium on respiration and locomotion in Lymnaea stagnalis (L.). J Exp Biol 213:1471-1476. CrossRef Medline
10. Dou JT, Chen M, Dufour F, Alkon DL, Zhao WQ (2005) Insulin receptor signaling in long-term memory consolidation following spatial learning. Learn Mem 12:646-655. CrossRef Medline
11. Elliott CJ, Vehovszky A (2000) Comparative pharmacology of feeding in molluscs. Acta Biol Hung 51:153-163. Medline
12. Fukuyama Y, Iwamoto S, Tanaka K (2006) Rapid sequencing and disulfide mapping of peptides containing disulfide bonds by using 1,5- diaminonaphthalene as a reductive matrix. J Mass Spectrom 41:191-201. Medline
13. Geraerts WP (1976a) Control of growth by the neurosecretory hormone of the light green cells in the freshwater snail Lymnaea stagnalis. Gen Comp Endocrinol 29:61-71. CrossRef Medline
14. Geraerts WP (1976b) The role of the lateral lobes in the control of growth and reproduction in the hermaphrodite freshwater snail Lymnaea stagnalis. Gen Comp Endocrinol 29:97-108. CrossRef Medline
15. Haj-ali V, Mohaddes G, Babri SH (2009) Intracerebroventricular insulin improves spatial learning and memory in male Wistar rats. Behav Neurosci 123:1309-1314. CrossRef Medline
16. Hatakeyama D, Ito I, Kojima S, Fujito Y, Ito E (2000) Complement receptor 3-like immunoreactivity in the light green cells and the canopy cells of the pond snail, Lymnaea stagnalis. Brain Res 865:102-106. CrossRef Medline
17. Inda MC, Delgado-García JM, Carrio ́n AM (2005) Acquisition, consolidation, reconsolidation, and extinction of eyelid conditioning responses require de novo protein synthesis. J Neurosci 25:2070-2080. CrossRef Medline
18. Ito E, Kobayashi S, Kojima S, Sadamoto H, Hatakeyama D (1999) Associative learning in the pond snail, Lymnaea stagnalis. Zool Sci 16:711-723. CrossRef
19. Ito E, Otsuka E, Hama N, Aonuma H, Okada R, Hatakeyama D, Fujito Y, Kobayashi S (2012a) Memory trace in feeding neural circuitry underlying conditioned taste aversion in Lymnaea. PLoS One 7:e43151. CrossRef Medline
20. Ito E, Okada R, Sakamoto Y, Otshuka E, Mita K, Okuta A, Sunada H, Sakakibara M (2012b) Insulin and memory in Lymnaea. Acta Biol Hung 63 [Suppl 2]:320-327.
21. Izquierdo LA, Barros DM, Ardenghi PG, Pereira P, Rodrigues C, Choi H, Medina JH, Izquierdo I (2000) Different hippocampal molecular requirements for short- and long-term retrieval of one-trial avoidance learning. Behav Brain Res 111:93-98. CrossRef Medline
22. Jonas EA, Knox RJ, Kaczmarek LK, Schwartz JH, Solomon DH (1996) Insulin receptor in Aplysia neurons: characterization, molecular cloning, and modulation of ion currents. J Neurosci 16:1645-1658. Medline
23. 2+ pool and of neuropeptide secretion. Nature 385:343-346. CrossRef Medline
24. Kawai R, Kobayashi S, Fujito Y, Ito E (2011) Multiple subtypes of serotonin receptors in the feeding circuit of a pond snail. Zool Sci 28:517-525. CrossRef Medline
25. Kemenes G, Benjamin PR (2009) Lymnaea. Curr Biol 19:R9-R11. CrossRef Medline
26. Kim JI, Lee HR, Sim SE, Baek J, Yu NK, Choi JH, Ko HG, Lee YS, Park SW, Kwak C, Ahn SJ, Choi SY, Kim H, Kim KH, Backx PH, Bradley CA, Kim E, Jang DJ, Lee K, Kim SJ, et al. (2011) PI3Kγ is required for NMDA receptor-dependent long-term depression and behavioral flexibility. Nat Neurosci 14:1447-1454. CrossRef Medline
27. Kits KS, de Vries NJ, Ebberink RH (1990) Molluscan insulin-related neuropeptide promotes neurite outgrowth in dissociated neuronal cell cultures. Neurosci Lett 109:253-258. CrossRef Medline
28. Kojima S, Yamanaka M, Fujito Y, Ito E (1996) Differential neuroethological effects of aversive and appetitive reinforcing stimuli on associative learning in Lymnaea stagnalis. Zool Sci 13:803-812. CrossRef
29. Kojima S, Nanakamura H, Nagayama S, Fujito Y, Ito E (1997) Enhancement of an inhibitory input to the feeding central pattern generator in Lymnaea stagnalis during conditioned taste-aversion learning. Neurosci Lett 230:179-182. CrossRef Medline
30. Kojima S, Hosono T, Fujito Y, Ito E (2001) Optical detection of neuromodulatory effects of conditioned taste aversion in the pond snail Lymnaea stagnalis. J Neurobiol 49:118-128. CrossRef Medline
31. Kyriakides MA, McCrohan CR (1989) Effect of putative neuromodulators on rhythmic buccal motor output in Lymnaea stagnalis. J Neurobiol 20: 635-650. CrossRef Medline
32. Lee YS, Bailey CH, Kandel ER, Kaang BK (2008) Transcriptional regulation of long-term memory in the marine snail Aplysia. Mol Brain 1:3. CrossRef Medline
33. Li KW, Geraerts WP, Ebberink RH, Joosse J (1992a) Purification and sequencing of molluscan insulin-related peptide I (MIP I) from the neuroendocrine light green cells of Lymnaea stagnalis. Mol Cell Endocrinol 85:141-150. CrossRef Medline
34. Li KW, Geraerts WP, Joosse J (1992b) Purification and sequencing of molluscan insulin-related peptide II from the neuroendocrine light green cells in Lymnaea stagnalis. Endocrinology 130:3427-3432. CrossRef Medline
35. Li KW, Geraerts WP, van Loenhout H, Joosse J (1992c) Biosynthesis and axonal transport of multiple molluscan insulin-related peptides by the neuroendocrine light green cells of Lymnaea stagnalis. Gen Comp Endocrinol 87:79-86. CrossRef Medline
36. Lukowiak K, Martens K, Rosenegger D, Browning K, de Caigny P, Orr M (2008) The perception of stress alters adaptive behaviours in Lymnaea stagnalis. J Exp Biol 211:1747-1756. CrossRef Medline
37. Matsumoto Y, Hatano A, Unoki S, Mizunami M (2009) Stimulation of the cAMP system by the nitric oxide-cGMP system underlying the formation of long-term memory in an insect. Neurosci Lett 467:81-85. CrossRef Medline
38. Matsuo R, Ito E (2009) A novel nitric oxide synthase expressed specifically in the olfactory center. Biochem Biophys Res Commun 386:724-728. CrossRef Medline
39. McCrohan CR, Benjamin PR (1980) Synaptic relationships of the cerebral giant cells with motor neurones in the feeding system of Lymnaea stagnalis. J Exp Biol 85:169-186. Medline
40. McNay EC, Ong CT, McCrimmon RJ, Cresswell J, Bogan JS, Sherwin RS (2010) Hippocampal memory processes are modulated by insulin and high-fat-induced insulin resistance. Neurobiol Learn Mem 93:546-553. CrossRef Medline
41. Meester I, Ramkema MD, van Minnen J, Boer HH (1992) Differential expression of four genes encoding molluscan insulin-related peptides in the central nervous system of the pond snail Lymnaea stagnalis. Cell Tissue Res 269:183-188. CrossRef Medline
42. Michel M, Green CL, Eskin A, Lyons LC (2011) PKG-mediated MAPK signaling is necessary for long-term operant memory in Aplysia. Learn Mem 18:108-117. CrossRef Medline
43. Murakami H, Bessinger K, Hellmann J, Murakami S (2005) Agingdependent and -independent modulation of associative learning behavior by insulin/insulin-like growth factor-1 signal in Caenorhabditis elegans. J Neurosci 25:10894-10904. CrossRef Medline
44. Nakamura H, Kojima S, Kobayashi S, Ito I, Fujito Y, Suzuki H, Ito E (1999a) Physiological characterization of lip and tentacle nerves in Lymnaea stagnalis. Neurosci Res 33:291-298. CrossRef Medline
45. Nakamura H, Kobayashi S, Kojima S, Urano A, Ito E (1999b) PKAdependent regulation of synaptic enhancement between a buccal motor neuron and its regulatory interneuron in Lymnaea stagnalis. Zool Sci 16:387-394. CrossRef
46. Nikitin ES, Vavoulis DV, Kemenes I, Marra V, Pirger Z, Michel M, Feng J, O'Shea M, Benjamin PR, Kemenes G (2008) Persistent sodium current is a nonsynaptic substrate for long-term associative memory. Curr Biol 18:1221-1226. CrossRef Medline
47. Oda S, Tomioka M, Iino Y (2011) Neuronal plasticity regulated by the insulin-like signaling pathway underlies salt chemotaxis learning in Caenorhabditis elegans. J Neurophysiol 106:301-308. CrossRef Medline
48. Ohnishi M, Matsumoto T, Nagashio R, Kageyama T, Utsuki S, Oka H, Okayasu I, Sato Y (2009) Proteomics of tumor-specific proteins in cerebrospinal fluid of patients with astrocytoma: usefulness of gelsolin protein. Pathol Int 59:797-803. CrossRef Medline
49. Orr MV, Hittel K, Lukowiak K (2009) "Different strokes for different folks": geographically isolated strains of Lymnaea stagnalis only respond to sympatric predators and have different memory forming capabilities. J Exp Biol 212:2237-2247. CrossRef Medline
50. Ramsey MM, Adams MM, Ariwodola OJ, Sonntag WE, Weiner JL (2005) Functional characterization of des-IGF-1 action at excitatory synapses in the CA1 region of rat hippocampus. J Neurophysiol 94:247-254. CrossRef Medline
51. Ribeiro MJ, Serfozo Z, Papp A, Kemenes I, O'Shea M, Yin JC, Benjamin PR, Kemenes G (2003) Cyclic AMP response element-binding (CREB)-like proteins in a molluscan brain: cellular localization and learning-induced phosphorylation. Eur J Neurosci 18:1223-1234. CrossRef Medline
52. Roovers E, Vincent ME, van Kesteren E, Geraerts WP, Planta RJ, Vreugdenhil E, van Heerikhuizen H (1995) Characterization of a putative molluscan insulin-related peptide receptor. Gene 162:181-188. CrossRef Medline
53. Rose RM, Benjamin PR (1979) The relationship of the central motor pattern to the feeding cycle of Lymnaea stagnalis. J Exp Biol 80:137-163. Medline
54. Rosenegger D, Wright C, Lukowiak K (2010) A quantitative proteomic analysis of long-term memory. Mol Brain 3:9. CrossRef Medline
55. Sadamoto H, Yamanaka M, Hatakeyama D, Nakamura H, Kojima S, Yamashita M, Ito E (2000) Developmental study of anatomical substrate for conditioned taste aversion in Lymnaea stagnalis. Zool Sci 17:141-148. CrossRef
56. Sadamoto H, Sato H, Kobayashi S, Murakami J, Aonuma H, Ando H, Fujito Y, Hamano K, Awaji M, Lukowiak K, Urano A, Ito E (2004) CREB in the pond snail Lymnaea stagnalis: cloning, gene expression, and function in identifiable neurons of the central nervous system. J Neurobiol 58:455-466. CrossRef Medline
57. Sadamoto H, Kitahashi T, Fujito Y, Ito E (2010) Learning-dependent gene expression of CREB1 isoforms in the molluscan brain. Front Behav Neurosci 4:25. Medline
58. Sadamoto H, Saito K, Muto H, Kinjo M, Ito E (2011) Direct observation of dimerization between different CREB1 isoforms in a living cell. PLoS One 6:e20285. CrossRef Medline
59. Sakakibara M (2006) Comparative study of visuo-vestibular conditioning in Lymnaea stagnalis. Biol Bull 210:298-307. CrossRef Medline
60. Sanna PP, Cammalleri M, Berton F, Simpson C, Lutjens R, Bloom FE, Francesconi W (2002) Phosphatidylinositol 3-kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region. J Neurosci 22:3359-3365. Medline
61. Smit AB, Vreugdenhil E, Ebberink RH, Geraerts WP, Klootwijk J, Joosse J (1988) Growth-controlling molluscan neurons produce the precur-sor of an insulin-related peptide. Nature 331:535-538. CrossRef Medline
62. Smit AB, Geraerts PM, Meester I, van Heerikhuizen H, Joosse J (1991) Characterization of a cDNA clone encoding molluscan insulin-related peptide II of Lymnaea stagnalis. Eur J Biochem 199:699-703. CrossRef Medline
63. Smit AB, Thijsen SF, Geraerts WP, Meester I, van Heerikhuizen H, Joosse J (1992) Characterization of a cDNA clone encoding molluscan insulinrelated peptide V of Lymnaea stagnalis. Brain Res Mol Brain Res 14:7-12. Medline
64. Smit AB, van Marle A, van Elk R, Bogerd J, van Heerikhuizen H, Geraerts WP (1993) Evolutionary conservation of the insulin gene structure in invertebrates: cloning of the gene encoding molluscan insulin-related peptide III from Lymnaea stagnalis. J Mol Endocrinol 11:103-113. CrossRef Medline
65. Smit AB, Spijker S, Van Minnen J, Burke JF, De Winter F, Van Elk R, Geraerts WP (1996) Expression and characterization of molluscan insulinrelated peptide VII from the mollusc Lymnaea stagnalis. Neuroscience 70:589-596. CrossRef Medline
66. Smit AB, van Kesteren RE, Li KW, Van Minnen J, Spijker S, Van Heerikhuizen H, Geraerts WP (1998) Towards understanding the role of insulin in the brain: lessons from insulin-related signaling systems in the invertebrate brain. Prog Neurobiol 54:35-54. CrossRef Medline
67. Smith MA, Riby LM, Eekelen JA, Foster JK (2011) Glucose enhancement of human memory: a comprehensive research review of the glucose memory facilitation effect. Neurosci Biobehav Rev 35:770-783. CrossRef Medline
68. Soos MA, Siddle K, Baron MD, Heward JM, Luzio JP, Bellatin J, Lennox ES (1986) Monoclonal antibodies reacting with multiple epitopes on the human insulin receptor. Biochem J 235:199-208. Medline
69. Straub VA, Staras K, Kemenes G, Benjamin PR (2002) Endogenous and network properties of Lymnaea feeding central pattern generator interneurons. J Neurophysiol 88:1569-1583. Medline
70. Straub VA, Kemenes I, O'Shea M, Benjamin PR (2006) Associative memory stored by functional novel pathway rather than modifications of preexisting neuronal pathways. J Neurosci 26:4139-4146. CrossRef Medline
71. Straub VA, Grant J, O'Shea M, Benjamin PR (2007) Modulation of serotonergic neurotransmission by nitric oxide. J Neurophysiol 97:1088-1099. Medline
72. Sugai R, Shiga H, Azami S, Watanabe T, Sadamoto H, Fujito Y, Lukowiak K, Ito E (2006) Taste discrimination in conditioned taste aversion of the pond snail Lymnaea stagnalis. J Exp Biol 209:826-833. CrossRef Medline
73. Sugai R, Azami S, Shiga H, Watanabe T, Sadamoto H, Kobayashi S, Hatakeyama D, Fujito Y, Lukowiak K, Ito E (2007) One-trial conditioned taste aversion in Lymnaea: good and poor performers in long-term memory acquisition. J Exp Biol 210:1225-1237. CrossRef Medline
74. Taylor R, Soos MA, Wells A, Argyraki M, Siddle K (1987) Insulin-like and insulin-inhibitory effects of monoclonal antibodies for different epitopes on the human insulin receptor. Biochem J 242:123-129. Medline
75. Tomioka M, Adachi T, Suzuki H, Kunitomo H, Schafer WR, Iino Y (2006) The insulin/PI 3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron 51:613-625. CrossRef Medline
76. Trannoy S, Redt-Clouet C, Dura JM, Preat T (2011) Parallel processing of appetitive short- and long-term memories in Drosophila. Curr Biol 21: 1647-1653. CrossRef Medline
77. Wagatsuma A, Sadamoto H, Kitahashi T, Lukowiak K, Urano A, Ito E (2005) Determination of the exact copy numbers of particular mRNAs in a single cell by quantitative real-time RT-PCR. J Exp Biol 208:2389-2398. CrossRef Medline
78. Wagatsuma A, Azami S, Sakura M, Hatakeyama D, Aonuma H, Ito E (2006) De Novo synthesis of CREB in a presynaptic neuron is required for synaptic enhancement involved in memory consolidation. J Neurosci Res 84:954-960. CrossRef Medline
79. Wan Q, Xiong ZG, Man HY, Ackerley CA, Braunton J, Lu WY, Becker LE, MacDonald JF, Wang YT (1997) Recruitment of functional GABAA receptors to postsynaptic domains by insulin. Nature 388:686-690. CrossRef Medline
80. Wu SP, Lu KT, Chang WC, Gean PW (1999) Involvement of mitogenactivated protein kinase in hippocampal long-term potentiation. J Biomed Sci 6:409-417. CrossRef Medline
81. Yeoman MS, Patel BA, Arundell M, Parker K, O'Hare D (2008) Synapsespecific changes in serotonin signalling contribute to age-related changes in the feeding behaviour of the pond snail, Lymnaea. J Neurochem 106: 1699-1709. CrossRef Medline
82. Zhao W, Chen H, Xu H, Moore E, Meiri N, Quon MJ, Alkon DL (1999) Brain insulin receptors and spatial memory. Correlated changes in gene expression, tyrosine phosphorylation, and signaling molecules in the hippocampus of water maze trained rats. J Biol Chem 274:34893-34902. CrossRef Medline