Activation of neurotensin receptor 1 facilitates neuronal excitability and spatial learning and memory in the entorhinal cortex: Beneficial actions in an Alzheimer's disease model

Journal of Neuroscience

Volumn 34, Issue 20, 2014, Pages 7027-7042

  Xiao, Zhaoyang ^a   Cilz, Nicholas I ^a   Kurada, Lalitha ^a   Hu, Binqi ^a   Yang, Chuanxiu ^a   Wada, Etsuko ^b   Combs, Colin K ^a   Porter, James E ^a   Lesage, Florian ^c   Lei, Saobo ^a  

^a UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^c INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Glutamate; Ion channel; Memory; Peptide; Synapse; Synaptic transmission

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; NEUROTENSIN RECEPTOR; NEUROTENSIN RECEPTOR 1; PROTEIN KINASE C; TANDEM PORE DOMAIN POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BARNES MAZE TEST; CONTROLLED STUDY; ENTORHINAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIAL; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MEMBRANE DEPOLARIZATION; NERVE CELL EXCITABILITY; NERVE POTENTIAL; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL LEARNING; SPATIAL MEMORY; WESTERN BLOTTING;

GLUTAMATE; ION CHANNEL; MEMORY; PEPTIDE; SYNAPSE; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ALZHEIMER DISEASE; ANIMALS; DISEASE MODELS, ANIMAL; ENTORHINAL CORTEX; MAZE LEARNING; MICE; NEURONS; NEUROTENSIN; RECEPTORS, NEUROTENSIN;

EID: 84900400954     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0408-14.2014     Document Type: Article

References (90)

1. Aller MI, Veale EL, Linden AM, Sandu C, Schwaninger M, Evans LJ, Korpi ER, Mathie A, Wisden W, Brickley SG (2005) Modifying the subunit composition of TASK channels alters the modulation of a leak conductance in cerebellar granule neurons. J Neurosci 25:11455-11467. CrossRef Medline
2. Alonso A, Klink R (1993) Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. J Neurophysiol 70:128-143. Medline
3. Atoji Y, Watanabe H, Yamamoto Y, Suzuki Y (1995) Distribution of neurotensin-containing neurons in the central nervous system of the dog. J Comp Neurol 353:67-88. CrossRef Medline
4. Azmi N, Norman C, Spicer CH, BennettGW (2006) Effects of a neurotensin analogue (PD149163) and antagonist (SR142948A) on the scopolamineinduced deficits in a novel object discrimination task. Behav Pharmacol 17:357-362. CrossRef Medline
5. + channel family. J Biol Chem 275:17412-17419. Medline
6. + channels. Mol Interv 3:205-219. CrossRef Medline
7. Bonini JS, Da Silva WC, Bevilaqua LR, Medina JH, Izquierdo I, Cammarota M (2007) On the participation of hippocampal PKC in acquisition, consolidation and reconsolidation of spatial memory. Neuroscience 147:37-45. CrossRef Medline
8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254. CrossRef Medline
9. Brandon MP, Bogaard AR, Libby CP, Connerney MA, Gupta K, Hasselmo ME (2011) Reduction of theta rhythm dissociates grid cell spatial periodicity from directional tuning. Science 332:595-599. CrossRef Medline
10. Breustedt J, Schmitz D, Heinemann U, Schmieden V (2004) Characterization of the inhibitory glycine receptor on entorhinal cortex neurons. Eur J Neurosci 19:1987-1991. CrossRef Medline
11. Burgalossi A, Herfst L, von Heimendahl M, Förste H, Haskic K, Schmidt M, BrechtM (2011) Microcircuits of functionally identified neurons in the rat medial entorhinal cortex. Neuron 70:773-786. CrossRef Medline
12. Canto CB, Wouterlood FG, Witter MP (2008) What does the anatomical organization of the entorhinal cortex tell us? Neural Plast 2008:381243. CrossRef Medline
13. Chen ST, Tsai MS, Shen CL (1988) Distribution of neurotensin-like immunoreactivity in the central nervous system of the Formosan monkey. Proc Natl Sci Counc Repub China B 12:163-173. Medline
14. Dash PK, Moore AN, Kobori N, Runyan JD (2007) Molecular activity underlying working memory. Learn Mem 14:554-563. CrossRef Medline
15. + channels. Mol Cell Neurosci 39:273-284. CrossRef Medline
16. Deng PY, Porter JE, Shin HS, Lei S (2006) Thyrotropin-releasing hormone increases GABA release in rat hippocampus. J Physiol 577:497-511. CrossRef Medline
17. + channels in the entorhinal cortex. Mol Pharmacol 72:208-218. CrossRef Medline
18. + channels. Neuron 63:230-243. CrossRef Medline
19. Deng PY, Xiao Z, Jha A, Ramonet D, Matsui T, Leitges M, Shin HS, Porter JE, Geiger JD, Lei S (2010) Cholecystokinin facilitates glutamate release by increasing the number of readily releasable vesicles and releasing probability. J Neurosci 30:5136-5148. CrossRef Medline
20. Dhawan G, Combs CK (2012) Inhibition of Src kinase activity attenuates amyloid associated microgliosis in a murine model of Alzheimer's disease. J Neuroinflammation 9:117. CrossRef Medline
21. Dickson CT, Mena AR, Alonso A (1997) Electroresponsiveness of medial entorhinal cortex layer III neurons in vitro. Neuroscience 81:937-950. CrossRef Medline
22. Dolcos F, LaBar KS, Cabeza R (2005) Remembering one year later: role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories. Proc Natl Acad Sci U S A 102:2626-2631. CrossRef Medline
23. Egorov AV, Hamam BN, Fransén E, Hasselmo ME, Alonso AA (2002) Graded persistent activity in entorhinal cortex neurons. Nature 420:173-178. CrossRef Medline
24. Faggin BM, Zubieta JK, Rezvani AH, Cubeddu LX (1990) Neurotensininduced dopamine release in vivo and in vitro from substantia nigra and nucleus caudate. J Pharmacol Exp Ther 252:817-825. Medline
25. Feifel D, Melendez G, Shilling PD (2004) Reversal of sensorimotor gating deficits in Brattleboro rats by acute administration of clozapine and a neurotensin agonist, but not haloperidol: a potential predictive model for novel antipsychotic effects. Neuropsychopharmacology 29:731-738. CrossRef Medline
26. Feifel D, Goldenberg J, Melendez G, Shilling PD (2010) The acute and subchronic effects of a brain-penetrating, neurotensin-1 receptor agonist on feeding, body weight and temperature. Neuropharmacology 58:195-198. CrossRef Medline
27. + channel. EMBO J 15:6854-6862. Medline
28. Garcia-Alloza M, Robbins EM, Zhang-Nunes SX, Purcell SM, Betensky RA, Raju S, Prada C, Greenberg SM, Bacskai BJ, Frosch MP (2006) Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 24:516-524. CrossRef Medline
29. Glogauer M, Arora P, Chou D, Janmey PA, Downey GP, McCulloch CA (1998) The role of actin-binding protein 280 in integrin-dependent mechanoprotection. J Biol Chem 273:1689-1698. Medline
30. Gómez-Isla T, Price JL, McKeel DW Jr, Morris JC, Growdon JH, Hyman BT (1996) Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J Neurosci 16:4491-4500. Medline
31. Gu W, Schlichthörl G, Hirsch JR, Engels H, Karschin C, Karschin A, Derst C, Steinlein OK, Daut J (2002) Expression pattern and functional characteristics of two novel splice variants of the two-pore-domain potassium channel TREK-2. J Physiol 539:657-668. CrossRef Medline
32. + channels. J Neurosci 29:2528-2533. CrossRef Medline
33. Hafting T, Fyhn M, Bonnevie T, Moser MB, Moser EI (2008) Hippocampusindependent phase precession in entorhinal grid cells. Nature 453:1248-1252. CrossRef Medline
34. Hamid EH, Hyde TM, Egan MF, Wolf SS, HermanMM, Nemeroff CB, Kleinman JE (2002) Neurotensin receptor binding abnormalities in the entorhinal cortex in schizophrenia and affective disorders. Biol Psychiatry 51:795-800. CrossRef Medline
35. Han J, Truell J, Gnatenco C, Kim D (2002) Characterization of four types of background potassium channels in rat cerebellar granule neurons. J Physiol 542:431-444. CrossRef Medline
36. Hermans E, Maloteaux JM (1998) Mechanisms of regulation of neurotensin receptors. Pharmacol Ther 79:89-104. CrossRef Medline
37. + channel involved in neuroprotection and general anesthesia. EMBO J 23:2684-2695. CrossRef Medline
38. Hu HJ, Gereau RW 4th (2003) ERK integrates PKA and PKC signaling in superficial dorsal horn neurons: II. Modulation of neuronal excitability. J Neurophysiol 90:1680-1688. CrossRef Medline
39. Huang D, Yu B (2008) Recent advance and possible future in TREK-2: a two-pore potassium channel may involved in the process of NPP, brain ischemia and memory impairment. Med Hypotheses 70:618-624. CrossRef Medline
40. Hyman BT, Van Hoesen GW, Damasio AR, Barnes CL (1984) Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science 225:1168-1170. CrossRef Medline
41. + channels and facilitates glutamatergic transmission in rat spinal cord dorsal horn. Eur J Neurosci 34:1230-1240. CrossRef Medline
42. + channel family. J Biol Chem 279:28063-28070. CrossRef Medline
43. Kang D, Han J, Kim D (2006) Mechanism of inhibition of TREK-2 (K2P10.1) by the Gq-coupled M3 muscarinic receptor. Am J Physiol Cell Physiol 291:C649-C656. CrossRef Medline
44. + channel family. J Biol Chem 275:9340-9347. CrossRef Medline
45. Kotzbauer PT, Trojanowsk JQ, LeeVM (2001) Lewy body pathology in Alzheimer's disease. J Mol Neurosci 17:225-232. CrossRef Medline
46. Kréneisz O, Benoit JP, Bayliss DA, Mulkey DK (2009) AMP-activated protein kinase inhibits TREK channels. J Physiol 587:5819-5830. CrossRef Medline
47. Kuzhikandathil EV, Oxford GS (2002) Classic D1 dopamine receptor antagonist R-(+)-7-chloro-8-hydroxy-3-methyl-1-phenyl-2,3,4,5-tetrahydro-1H-3-benzazepine hydrochloride (SCH23390) directly inhibits G protein-coupled inwardly rectifying potassium channels. Mol Pharmacol 62:119-126. CrossRef Medline
48. 3H]Neurotensin receptor densities in human postmortem brain tissue obtained from normal and schizophrenic persons: an autoradiographic study. J Neural Transm 105:507-516. CrossRef Medline
49. Lapchak PA, Araujo DM, Quirion R, Beaudet A (1990) Neurotensin regulation of endogenous acetylcholine release from rat cerebral cortex: effect of quinolinic acid lesions of the basal forebrain. J Neurochem 55:1397-1403. CrossRef Medline
50. Lapchak PA, Araujo DM, Quirion R, Beaudet A (1991) Neurotensin regulation of endogenous acetylcholine release from rat striatal slices is independent of dopaminergic tone. J Neurochem 56:651-657. CrossRef Medline
51. László K, Tóth K, Kertes E, Péczely L, Ollmann T, Lénárd L (2010) Effects of neurotensin in amygdaloid spatial learning mechanisms. Behav Brain Res 210:280-283. CrossRef Medline
52. Lei S (2012) Serotonergic modulation of neural activities in the entorhinal cortex. Int J Physiol Pathophysiol Pharmacol 4:201-210. Medline
53. Lei S, Deng PY, Porter JE, Shin HS (2007) Adrenergic facilitation of GABAergic transmission in rat entorhinal cortex. J Neurophysiol 98:2868-2877. CrossRef Medline
54. Lesage F (2003) Pharmacology of neuronal background potassium channels. Neuropharmacology 44:1-7. CrossRef Medline
55. Lesage F, Lazdunski M (2000) Molecular and functional properties of twopore-domain potassium channels. Am J Physiol Renal Physiol 279:F793-F801. Medline
56. + channel with a novel structure. EMBO J 15:1004-1011. Medline
57. Li J, Chen C, Chen C, He Q, Li H, Li J, Moyzis RK, Xue G, Dong Q (2011) Neurotensin receptor 1 gene (NTSR1) polymorphism is associated with working memory. PLoS One 6:e17365. CrossRef Medline
58. +-ATPase activity through high affinity peptide receptor. Peptides 21:571-576. CrossRef Medline
59. 2+ block of the two-pore domain potassium channel TREK-1 defines conformational transition in its selectivity filter. J Biol Chem 286:39813-39822. CrossRef Medline
60. Maeno H, Yamada K, Santo-Yamada Y, Aoki K, Sun YJ, Sato E, Fukushima T, Ogura H, Araki T, Kamichi S, Kimura I, Yamano M, Maeno-Hikichi Y, Watase K, Aoki S, Kiyama H, Wada E, Wada K (2004) Comparison of mice deficient in the high-or low-affinity neurotensin receptors, Ntsr1 or Ntsr2, reveals a novel function for Ntsr2 in thermal nociception. Brain Res 998:122-129. CrossRef Medline
61. Martorana A, Martella G, D'Angelo V, Fusco FR, Spadoni F, Bernardi G, Stefani A (2006) Neurotensin effects on N-type calcium currents among rat pallidal neurons: an electrophysiological and immunohistochemical study. Synapse 60:371-383. CrossRef Medline
62. Nishimura R, Kato Y, Chen D, Harris SE, Mundy GR, Yoneda T (1998) Smad5 and DPC4 are key molecules in mediating BMP-2-induced osteoblastic differentiation of the pluripotent mesenchymal precursor cell line C2C12. J Biol Chem 273:1872-1879. CrossRef Medline
63. O'Connor WT, Tanganelli S, Ungerstedt U, Fuxe K (1992) The effects of neurotensin on GABA and acetylcholine release in the dorsal striatum of the rat: an in vivo microdialysis study. Brain Res 573:209-216. CrossRef Medline
64. Ohinata K, Sonoda S, Inoue N, Yamauchi R, Wada K, Yoshikawa M (2007) β-Lactotensin, a neurotensin agonist peptide derived from bovine β-lactoglobulin, enhances memory consolidation in mice. Peptides 28: 1470-1474. CrossRef Medline
65. Pan YP, Xu XH, Wang XL (2003) [mRNA expression alteration of two-pore potassium channels in the brain of beta-amyloid peptide25-35-induced memory impaired rats]. Yao Xue Xue Bao 38:721-724. Medline
66. Pepeu G, Giovannini MG (2009) Cholinesterase inhibitors and beyond. Curr Alzheimer Res 6:86-96. CrossRef Medline
67. Petkova-Kirova P, Rakovska A, Della Corte L, Zaekova G, Radomirov R, Mayer A (2008) Neurotensin modulation of acetylcholine, GABA, and aspartate release from rat prefrontal cortex studied in vivo with microdialysis. Brain Res Bull 77:129-135. CrossRef Medline
68. Rakovska A, Giovannini MG, Della Corte L, Kalfin R, Bianchi L, Pepeu G (1998) Neurotensin modulation of acetylcholine and GABA release from the rat hippocampus: an in vivo microdialysis study. Neurochem Int 33: 335-340. CrossRef Medline
69. Ramanathan G, Cilz NI, Kurada L, Hu B, Wang X, Lei S (2012) Vasopressin facilitates GABAergic transmission in rat hippocampus via activation of V1A receptors. Neuropharmacology 63:1218-1226. CrossRef Medline
70. 14C]acetylcholine in the rat nucleus accumbens. Neurochem Res 17:1143-1146. CrossRef Medline
71. Rowe WB, Kar S, Meaney MJ, Quirion R (2006) Neurotensin receptor levels as a function of brain aging and cognitive performance in the Morris water maze task in the rat. Peptides 27:2415-2423. CrossRef Medline
72. + channel, TRESK, is localized in the spinal cord. J Biol Chem 278: 27406-27412. CrossRef Medline
73. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser MB, Moser EI (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312:758-762. CrossRef Medline
74. Steffenach HA, Witter M, Moser MB, Moser EI (2005) Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45:301-313. CrossRef Medline
75. St-Gelais F, Jomphe C, Trudeau LE (2006) The role of neurotensin in central nervous system pathophysiology: what is the evidence? J Psychiatry Neurosci 31:229-245. Medline
76. Sun MK, Alkon DL (2010) Pharmacology of protein kinase C activators: cognition-enhancing and antidementic therapeutics. Pharmacol Ther 127:66-77. CrossRef Medline
77. Tirado-Santiago G, Lázaro-Muñoz G, Rodríguez-González V, Maldonado-Vlaar CS (2006) Microinfusions of neurotensin antagonist SR 48692 within the nucleus accumbens core impair spatial learning in rats. Behav Neurosci 120:1093-1102. CrossRef Medline
78. van Marum RJ (2008) Current and future therapy in Alzheimer's disease. Fundam Clin Pharmacol 22:265-274. CrossRef Medline
79. Vincent JP, Mazella J, Kitabgi P (1999) Neurotensin and neurotensin receptors. Trends Pharmacol Sci 20:302-309. CrossRef Medline
80. Wang S, Zhang AP, Kurada L, Matsui T, Lei S (2011) Cholecystokinin facilitates neuronal excitability in the entorhinal cortex via activation of TRPC-like channels. J Neurophysiol 106:1515-1524. CrossRef Medline
81. Wang S, Chen X, Kurada L, Huang Z, Lei S (2012) Activation of group II metabotropic glutamate receptors inhibits glutamatergic transmission in the rat entorhinal cortex via reduction of glutamate release probability. Cereb Cortex 22:584-594. CrossRef Medline
82. Wang S, Kurada L, Cilz NI, Chen X, Xiao Z, Dong H, Lei S (2013) Adenosinergic depression of glutamatergic transmission in the entorhinal cortex of juvenile rats via reduction of glutamate release probability and the number of releasable vesicles. PLoS One 8:e62185. CrossRef Medline
83. Watanabe M, Nakamura M, Sato K, Kano M, Simon MI, Inoue Y (1998) Patterns of expression for the mRNA corresponding to the four isoforms of phospholipase Cbeta in mouse brain. Eur J Neurosci 10:2016-2025. CrossRef Medline
84. 125I-neurotensin binding sites in human entorhinal cortex. Brain Res Bull 35:353-358. CrossRef Medline
85. Wolf SS, Hyde TM, Saunders RC, Herman MM, Weinberger DR, Kleinman JE (1995) Autoradiographic characterization of neurotensin receptors in the entorhinal cortex of schizophrenic patients and control subjects. J Neural Transm Gen Sect 102:55-65. CrossRef Medline
86. + channels. J Biol Chem 284:10980-10991. CrossRef Medline
87. Yagi K, Goto D, Hamamoto T, Takenoshita S, Kato M, Miyazono K (1999) Alternatively spliced variant of Smad2 lacking exon 3: comparison with wild-type Smad2 and Smad3. J Biol Chem 274:703-709. CrossRef Medline
88. Yamauchi R, Wada E, Kamichi S, Yamada D, Maeno H, Delawary M, Nakazawa T, Yamamoto T, Wada K (2007) Neurotensin type 2 receptor is involved in fear memory in mice. J Neurochem 102:1669-1676. CrossRef Medline
89. Yin HH, Adermark L, Lovinger DM (2008) Neurotensin reduces glutamatergic transmission in the dorsolateral striatum via retrograde endocannabinoid signaling. Neuropharmacology 54:79-86. CrossRef Medline
90. Zhang HP, Xiao Z, Cilz NI, Hu B, Dong H, Lei S (2014) Bombesin facilitates GABAergic transmission and depresses epileptiform activity in the entorhinal cortex. Hippocampus 24:21-31. CrossRef Medline