Oxytocin promotes long-term potentiation by enhancing epidermal growth factor receptor-mediated local translation of protein kinase Mς

Journal of Neuroscience

Volumn 32, Issue 44, 2012, Pages

  Lin, Yu Ting ^a   Huang, Chiung Chun ^a   Hsu, Kuei Sen ^a  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; OXYTOCIN; OXYTOCIN RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE C; PROTEIN KINASE M ZETA; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SYNAPTOSOME; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYO; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; HIPPOCAMPAL CA1 REGION; LONG TERM POTENTIATION; MALE; MUSCLE TETANIC CONTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS REGULATION; RAT; RNA TRANSLATION; SIGNAL TRANSDUCTION; SPIKE WAVE; WESTERN BLOTTING;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CELLS, CULTURED; DENDRITES; ELECTRIC STIMULATION; FEMALE; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MAP KINASE SIGNALING SYSTEM; OXYTOCIN; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN BIOSYNTHESIS; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, EPIDERMAL GROWTH FACTOR; SYNAPTOSOMES; TYPE C PHOSPHOLIPASES;

EID: 84868124538     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2429-12.2012     Document Type: Article

References (70)

1. Balkowiec A, Katz DM (2002) Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J Neurosci 22:10399-10407. Medline
2. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39. CrossRef Medline
3. Borrell J, De Kloet ER, Versteeg DH, Bohus B (1983) Inhibitory avoidance deficit following short-term adrenalectomy in the rat: the role of adrenal catecholamines. Behav Neural Biol 39:241-258. CrossRef Medline
4. Brown EJ, Schreiber SL (1996) A signaling pathway to translational control. Cell 86:517-520. CrossRef Medline
5. Buijs RM, Swaab DF (1979) Immuno-electron microscopical demonstration of vasopressin and oxytocin synapses in the limbic system of the rat. Cell Tissue Res 204:355-365. Medline
6. Cattaneo MG, Lucci G, Vicentini LM (2009) Oxytocin stimulates in vitro angiogenesis via a Pyk-2/Src-dependent mechanism. Exp Cell Res 315: 3210-3219. CrossRef Medline
7. Chandler LJ, Sutton G, Dorairaj NR, Norwood D (2001) N-methyl-Daspartate receptor-mediated bidirectional control of extracellular signal-regulated kinase activity in cortical neuronal cultures. J Biol Chem 276: 2627-2636. CrossRef Medline
8. Chiu T, Santiskulvong C, Rozengurt E (2005) EGF receptor transactivation mediates ANG II-stimulated mitogenesis in intestinal epithelial cells through the PI3-kinase/Akt/mTOR/p70S6K1 signaling pathway. Am J Physiol Gastrointest Liver Physiol 288:G182-G194. CrossRef Medline
9. Cohen H, Kaplan Z, Kozlovsky N, Gidron Y, Matar MA, Zohar J (2010) Hippocampal microinfusion of oxytocin attenuates the behavioural response to stress by means of dynamic interplay with the glucocorticoid-catecholamine responses. J Neuroendocrinol 22:889-904. Medline
10. Deadwyler SA, Dunwiddie T, Lynch G (1987) A critical level of protein synthesis is required for long-term potentiation. Synapse 1:90-95. CrossRef Medline
11. de Oliveira LF, Camboim C, Diehl F, Consiglio AR, Quillfeldt JA (2007) Glucocorticoid-mediated effects of systemic oxytocin upon memory retrieval. Neurobiol Learn Mem 87:67-71. CrossRef Medline
12. Dubrovsky B, Harris J, Gijsbers K, Tatarinov A (2002) Oxytocin induces long-term depression on the rat dentate gyrus: possible ATPase and ectoprotein kinase mediation. Brain Res Bull 58:141-147. CrossRef Medline
13. Fang LY, Quan RD, Kaba H (2008) OxytocDubrovskyin facilitates the induction of long-term potentiation in the accessory olfactory bulb. Neurosci Lett 438:133-137. CrossRef Medline
14. Ferguson JN, Young LJ, Hearn EF, Matzuk MM, Insel TR, Winslow JT (2000) Social amnesia in mice lacking the oxytocin gene. Nat Genet 25: 284-288. CrossRef Medline
15. Franke TF, Yang SI, Chan TO, Datta K, Kazlauskas A, Morrison DK, Kaplan DR, Tsichlis PN (1995) The protein kinase encoded by the Akt protooncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81:727-736. CrossRef Medline
16. Frey U, Krug M, Reymann KG, Matthies H (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452:57-65. CrossRef Medline
17. Gainer H, Wray S (1992) Oxytocin and vasopressin. From genes to peptides. Ann N Y Acad Sci 652:14-28. CrossRef Medline
18. Gimpl G, Fahrenholz F (2001) The oxytocin receptor system: structure, function, and regulation. Physiol Rev 81:629-683. Medline
19. Gold PE (1986) The use of avoidance training in studies of modulation of memory storage. Behav Neural Biol 46:87-98. CrossRef Medline
20. Hardt O, Migues PV, Hastings M, Wong J, Nader K (2010) PKM maintains 1-day-and 6-day-old long-term object location but not object identity memory in dorsal hippocampus. Hippocampus 20:691-695. Medline
21. Hollingsworth EB, McNeal ET, Burton JL, Williams RJ, Daly JW, Creveling CR (1985) Biochemical characterization of a filtered synaptoneurosome preparation from guinea pig cerebral cortex: cyclic adenosine 3:5-monophosphate-generating systems, receptors, and enzymes. J Neurosci 5:2240-2253. Medline
22. Huang CC, Hsu KS (2006) Sustained activation of metabotropic glutamate receptor 5 and protein tyrosine phosphatases mediate the expression of (S)-3,5-dihydroxyphenylglycine-induced long-term depression in the hippocampal CA1 region. J Neurochem 96:179-194. CrossRef Medline
23. Huang YF, Yang CH, Huang CC, Tai MH, Hsu KS (2010) Pharmacological and genetic accumulation of hypoxia-inducible factor-1α enhances excitatory synaptic transmission in hippocampal neurons through the production of vascular endothelial growth factor. J Neurosci 30:6080-6093. CrossRef Medline
24. Huttner WB, Schiebler W, Greengard P, De Camilli P (1983) Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol 96:1374-1388. CrossRef Medline
25. Insel TR, Gelhard R, Shapiro LE (1991) The comparative distribution of forebrain receptors for neurohypophyseal peptides in monogamous and polygamous mice. Neuroscience 43:623-630. CrossRef Medline
26. Kalmes A, Vesti BR, Daum G, Abraham JA, Clowes AW (2000) Heparin blockade of thrombin-induced smooth muscle cell migration involves inhibition of epidermal growth factor (EGF) receptor transactivation by heparin-binding EGF-like growth factor. Circ Res 87:92-98. CrossRef Medline
27. Kelleher RJ 3rd, Govindarajan A, Tonegawa S (2004) Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44:59-73. CrossRef Medline
28. Kelly MT, Crary JF, Sacktor TC (2007) Regulation of protein kinase M synthesis by multiple kinases in long-term potentiation. J Neurosci 27: 3439-3444. CrossRef Medline
29. Krishnaswamy N, Lacroix-Pepin N, Chapdelaine P, Taniguchi H, Kauffenstein G, Chakravarti A, Danyod G, Fortier MA (2010) Epidermal growth factor receptor is an obligatory intermediate for oxytocin-induced cyclooxygenase 2 expression and prostaglandin F2 alpha production in bovine endometrial epithelial cells. Endocrinology 151:1367-1374. CrossRef Medline
30. Laudanna C, Mochly-Rosen D, Liron T, Constantin G, Butcher EC (1998) Evidence of protein kinase C involvement in polymorphonuclear neutrophil integrin-dependent adhesion and chemotaxis. J Biol Chem 273: 30306-30315. CrossRef Medline
31. Lee HJ, Macbeth AH, Pagani JH, Young WS 3rd (2009) Oxytocin: the great facilitator of life. Prog Neurobiol 88:127-151. Medline
32. Leuner B, Caponiti JM, Gould E (2012) Oxytocin stimulates adult neurogenesis even under conditions of stress and elevated glucocorticoids. Hippocampus 22:861-868. CrossRef Medline
33. Levitzki A, Gazit A (1995) Tyrosine kinase inhibition: an approach to drug development. Science 267:1782-1788. CrossRef Medline
34. Lin HJ, Huang CC, Hsu KS (2006) Effects of neonatal dexamethasone treatment on hippocampal synaptic function. Ann Neurol 59:939-951. CrossRef Medline
35. Ling DS, Benardo LS, Serrano PA, Blace N, Kelly MT, Crary JF, Sacktor TC (2002) Protein kinase M is necessary and sufficient for LTP maintenance. Nat Neurosci 5:295-296. CrossRef Medline
36. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649-711. CrossRef Medline
37. Meyer-Lindenberg A, Domes G, Kirsch P, Heinrichs M (2011) Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat Rev Neurosci 12:524-538. CrossRef Medline
38. Monks DA, Lonstein JS, Breedlove SM (2003) Got milk? Oxytocin triggers hippocampal plasticity. Nat Neurosci 6:327-328. CrossRef Medline
39. Muslimov IA, Nimmrich V, Hernandez AI, Tcherepanov A, Sacktor TC, Tiedge H (2004) Dendritic transport and localization of protein kinase M mRNA: implications for molecular memory consolidation. J Biol Chem 279:52613-52622. CrossRef Medline
40. Naik MU, Benedikz E, Hernandez I, Libien J, Hrabe J, Valsamis M, Dow-Edwards D, Osman M, Sacktor TC (2000) Distribution of protein kinase M and the complete protein kinase C isoform family in rat brain. J Comp Neurol 426:243-258. CrossRef Medline
41. Neumann ID (2008) Brain oxytocin: a key regulator of emotional and social behaviors in both females and males. J Neuroendocrinol 20:858-865. CrossRef Medline
42. Neumann ID, Landgraf R (2008) Advances in vasopressin and oxytocin-from genes to behavior to disease. Prog Brain Res 170:xi-xiii. CrossRef Medline
43. Nguyen PV, Abel T, Kandel ER (1994) Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265:1104-1107. CrossRef Medline
44. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC (2006) Storage of spatial information by the maintenance mechanism of LTP. Science 313:1141-1144. CrossRef Medline
45. Pedersen CA, Prange AJ Jr (1979) Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc Natl Acad Sci U S A 76:6661-6665. CrossRef Medline
46. Perkinton MS, Ip JK, Wood GL, Crossthwaite AJ, Williams RJ (2002) Phosphatidylinositol 3-kinase is a central mediator of NMDA receptor signalling to MAP kinase (Erk1/2), Akt/PKB and CREB in striatal neurones. J Neurochem 80:239-254. CrossRef Medline
47. Prenzel N, Zwick E, Daub H, Leserer M, Abraham R, Wallasch C, Ullrich A (1999) EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402:884-888. Medline
48. Raab G, Klagsbrun M (1997) Heparin-binding EGF-like growth factor. Biochim Biophys Acta 1333:F179-F199. Medline
49. Rao A, Steward O (1991) Evidence that protein constituents of postsynaptic membrane specializations are locally synthesized: analysis of proteins synthesized within synaptosomes. J Neurosci 11:2881-2895. Medline
50. Sacktor TC (2011) How does PKM maintain long-term memory? Nat Rev Neurosci 12:9-15. CrossRef Medline
51. Sacktor TC, Osten P, Valsamis H, Jiang X, Naik MU, Sublette E (1993) Persistent activation of the isoform of protein kinase C in the maintenance of long-term potentiation. Proc Natl Acad Sci U S A 90:8342-8346. CrossRef Medline
52. Sajikumar S, Navakkode S, Sacktor TC, Frey JU (2005) Synaptic tagging and cross-tagging: the role of protein kinase M in maintaining long-term potentiation but not long-term depression. J Neurosci 25:5750-5756. CrossRef Medline
53. Serrano P, Yao Y, Sacktor TC (2005) Persistent phosphorylation by protein kinase M maintains late-phase long-term potentiation. J Neurosci 25: 1979-1984. CrossRef Medline
54. Serrano P, Friedman EL, Kenney J, Taubenfeld SM, Zimmerman JM, Hanna J, Alberini C, Kelley AE, Maren S, Rudy JW, Yin JC, Sacktor TC, Fenton AA (2008) PKM maintains spatial, instrumental, and classically conditioned long-term memories. PLoS Biol 6:2698-2706. Medline
55. Sofroniew MV (1983) Morphology of vasopressin and oxytocin neurons and their central and vascular projections. Prog Brain Res 60:101-114. CrossRef Medline
56. Stanton PK, Sarvey JM (1984) Blockade of long-term potentiation in rat hippocampal CA1 region by inhibitors of protein synthesis. J Neurosci 4:3080-3088. Medline
57. Stoica L, Zhu PJ, Huang W, Zhou H, Kozma SC, Costa-Mattioli M (2011) Selective pharmacogenetic inhibition of mammalian target of Rapamycin complex I (mTORC1) blocks long-term synaptic plasticity and memory storage. Proc Natl Acad Sci U S A 108:3791-3796. CrossRef Medline
58. Tang SJ, Reis G, Kang H, Gingras AC, Sonenberg N, Schuman EM (2002) A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc Natl Acad Sci U S A 99:467-472. CrossRef Medline
59. Tapley P, Lamballe F, Barbacid M (1992) K252a is a selective inhibitor of the tyrosine protein kinase activity of the trk family of oncogenes and neurotrophin receptors. Oncogene 7:371-381. Medline
60. Tomizawa K, Iga N, Lu YF, Moriwaki A, Matsushita M, Li ST, Miyamoto O, Itano T, Matsui H (2003) Oxytocin improves long-lasting spatial memory during motherhood through MAP kinase cascade. Nat Neurosci 6:384-390. CrossRef Medline
61. Tsokas P, Grace EA, Chan P, Ma T, Sealfon SC, Iyengar R, Landau EM, Blitzer RD (2005) Local protein synthesis mediates a rapid increase in dendritic elongation factor 1A after induction of late long-term potentiation. J Neurosci 25:5833-5843. CrossRef Medline
62. Tyzio R, Cossart R, Khalilov I, Minlebaev M, Hubner CA, Represa A, Ben-Ari Y, Khazipov R (2006) Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 314: 1788-1792. CrossRef Medline
63. Veinante P, Freund-Mercier MJ (1997) Distribution of oxytocin-and vasopressin-binding sites in the rat extended amygdala: a histoautoradiographic study. J Comp Neurol 383:305-325. Medline
64. Wigström H, Gustafsson B (1983) Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition. Nature 301:603-604. CrossRef Medline
65. Yang PC, Yang CH, Huang CC, Hsu KS (2008) Phosphatidylinositol 3-kinase activation is required for stress protocol-induced modification of hippocampal synaptic plasticity. J Biol Chem 283:2631-2643. Medline
66. Yao Y, Kelly MT, Sajikumar S, Serrano P, Tian D, Bergold PJ, Frey JU, Sacktor TC (2008) PKM maintains late long-term potentiation by N-ethylmaleimide-sensitive factor/GluR2-dependent trafficking of postsynaptic AMPA receptors. J Neurosci 28:7820-7827. CrossRef Medline
67. Young WS 3rd, Gainer H (2003) Transgenesis and the study of expression, cellular targeting and function of oxytocin, vasopressin and their receptors. Neuroendocrinology 78:185-203. CrossRef Medline
68. Zaninetti M, Raggenbass M (2000) Oxytocin receptor agonists enhance inhibitory synaptic transmission in the rat hippocampus by activating interneurons in stratum pyramidale. Eur J Neurosci 12:3975-3984. CrossRef Medline
69. βγ and epidermal growth factor receptor tyrosine kinase activation. Endocrinology 144:2947-2956. CrossRef Medline
70. Zwick E, Wallasch C, Daub H, Ullrich A (1999) Distinct calcium-dependent pathways of epidermal growth factor receptor transactivation and Pyk2 tyrosine phosphorylation in PC12 cells. J Biol Chem 274:20989-20996. CrossRef Medline