Increase in cortical endocannabinoid signaling in a rat model of basal forebrain cholinergic dysfunction

Neuroscience

Volumn 362, Issue , 2017, Pages 206-218

  Llorente Ovejero, Alberto ^a   Manuel, Iván ^a   Giralt, Maria Teresa ^a   Rodríguez Puertas, Rafael ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

192IgG saporin; autoradiography; CB1 receptors; GABA; memory; nucleus basalis magnocellularis

Indexed keywords

CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; 192 IGG-SAPORIN; 4 AMINOBUTYRIC ACID; CNR1 PROTEIN, RAT; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 2; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); MONOCLONAL ANTIBODY; NERVE GROWTH FACTOR RECEPTOR; RIBOSOME INACTIVATING PROTEIN 1; TNFRSF16 PROTEIN, RAT;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; CELLULAR DISTRIBUTION; CHOLINERGIC SYSTEM; CONTROLLED STUDY; DENERVATION; DOWN REGULATION; HIPPOCAMPUS; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; LIMIT OF QUANTITATION; MALE; NEUROTRANSMISSION; NONHUMAN; NUCLEUS BASALIS MAGNOCELLULARIS; PASSIVE AVOIDANCE TEST; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; ANIMAL; BASAL FOREBRAIN; BRAIN CORTEX; CHOLINERGIC NERVE CELL; DISEASE MODEL; LEARNING DISORDER; MEMORY DISORDER; METABOLISM; PATHOLOGY; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ANIMALS; ANTIBODIES, MONOCLONAL; BASAL FOREBRAIN; CEREBRAL CORTEX; CHOLINERGIC NEURONS; DISEASE MODELS, ANIMAL; ENDOCANNABINOIDS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); LEARNING DISORDERS; MALE; MEMORY DISORDERS; RANDOM ALLOCATION; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; RECEPTORS, NERVE GROWTH FACTOR; RIBOSOME INACTIVATING PROTEINS, TYPE 1;

EID: 85029124857     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2017.08.008     Document Type: Article

References (70)

1. Albayram, O., Alferink, J., Pitsch, J., Piyanova, A., Neitzert, K., Poppensieker, K., Mauer, D., Michel, K., Legler, A., Becker, A., Monory, K., Lutz, B., Zimmer, A., Bilkei-Gorzo, A., Role of CB1 cannabinoid receptors on GABAergic neurons in brain aging. Proc Natl Acad Sci U S A 108:27 (2011), 11256–11261
2. Anglade, F., Bizot, J.C., Dodd, R.H., Baudoin, C., Chapouthier, G., Opposite effects of cholinergic agents and benzodiazepine receptor ligands in a passive avoidance task in rats. Neurosci Lett 182:2 (1994), 247–250
3. Auclair, N., Otani, S., Soubrie, P., Crepel, F., Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefrontal cortex pyramidal neurons. J Neurophysiol 83:6 (2000), 3287–3293
4. Barreda-Gómez, G., Lombardero, L., Giralt, M.T., Manuel, I., Rodríguez-Puertas, R., Effects of galanin subchronic treatment on memory and muscarinic receptors. Neuroscience 293 (2015), 23–34
5. Bartus, R.T., Dean, R.L., Beer, B., Lippa, A.S., The cholinergic hypothesis of geriatric memory dysfunction. Science 217:4558 (1982), 408–414
6. Benito, C., Núñez, E., Tolón, R.M., Carrier, E.J., Rábano, A., Hillard, C.J., Romero, J., Cannabinoid CB2 receptors and fatty acid amide hydrolase are selectively overexpressed in neuritic plaque-associated glia in Alzheimer's disease brains. J Neurosci 23:35 (2003), 11136–11141
7. Bilkei-Gorzo, A., Albayram, O., Draffehn, A., Michel, K., Piyanova, A., Oppenheimer, H., Dvir-Ginzberg, M., Rácz, I., Ulas, T., Imbeault, S., Bab, I., Schultze, J.L., Zimmer, A., A chronic low dose of Δ9-tetrahydrocannabinol (THC) restores cognitive function in old mice. Nat Med 6 (2017), 782–787
8. Busquets-Garcia, A., Puighermanal, E., Pastor, A., de la Torre, R., Maldonado, R., Ozaita, A., Differential role of anandamide and 2-arachidonoylglycerol in memory and anxiety-like responses. Biol Psychiatry 70:5 (2011), 479–486
9. Busquets-Garcia, A., Gomis-González, M., Srivastava, R.K., Cutando, L., Ortega-Alvaro, A., Ruehle, S., Remmers, F., Bindila, L., Bellocchio, L., Marsicano, G., Lutz, B., Maldonado, R., Ozaita, A., Peripheral and central CB1 cannabinoid receptors control stress-induced impairment of memory consolidation. Proc Natl Acad Sci U S A 113:35 (2016), 9904–9909
10. Chiarlone, A., Bellocchio, L., Blázquez, C., Resel, E., Soria-Gómez, E., Cannich, A., Ferrero, J.J., Sagredo, O., Benito, C., Romero, J., Sánchez-Prieto, J., Lutz, B., Fernández-Ruiz, J., Galve-Roperh, I., Guzmán, M., A restricted population of CB1 cannabinoid receptors with neuroprotective activity. Proc Natl Acad Sci U S A 111:22 (2014), 8257–8262
11. Chugh, Y., Saha, N., Sankaranarayanan, A., Sharma, P.L., Possible mechanism of haloperidol-induced enhancement of memory retrieval. Methods Find Exp Clin Pharmacol 13:3 (1991), 161–164
12. Conner, J.M., Chiba, A.A., Tuszynski, M.H., The basal forebrain cholinergic system is essential for cortical plasticity and functional recovery following brain injury. Neuron 46:2 (2005), 173–179
13. Cui, Y., Costa, R.M., Murphy, G.G., Elgersma, Y., Zhu, Y., Gutmann, D.H., Parada, L.F., Mody, I., Silva, A.J., Neurofibromin regulation of ERK signaling modulates GABA release and learning. Cell 135:3 (2008), 549–560
14. Cummings, J., Lai, T.J., Hemrungrojn, S., Mohandas, E., Yun Kim, S., Nair, G., Dash, A., Role of donepezil in the management of neuropsychiatric symptoms in Alzheimer's disease and dementia with Lewy bodies. CNS Neurosci Ther, 2016, 1–8
15. D'Addario, C., Di Francesco, A., Arosio, B., Gussago, C., Dell'Osso, B., Bari, M., Galimberti, D., Scarpini, E., Altamura, A.C., Mari, D., Maccarrone, M., Epigenetic regulation of fatty acid amide hydrolase in Alzheimer disease. PLoS One, 7(6), 2012, e39186
16. Davies, P., Neurotransmitter-related enzymes in senile dementia of the Alzheimer type. Brain Res 171:2 (1979), 319–327
17. Davies, P., Maloney, A.J., Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet, 2(8000), 1976, 1403
18. Doyle, E., Regan, C.M., Cholinergic and dopaminergic agents which inhibit a passive avoidance response attenuate the paradigm-specific increases in NCAM sialylation state. J Neural Transm Gen Sec 92:1 (1993), 33–49
19. Fukudome, Y., Ohno-Shosaku, T., Matsui, M., Omori, Y., Fukaya, M., Tsubokawa, H., Taketo, M.M., Watanabe, M., Manabe, T., Kano, M., Two distinct classes of muscarinic action on hippocampal inhibitory synapses: M2-mediated direct suppression and M1/M3-mediated indirect suppression through endocannabinoid signalling. Eur J Neurosci 19:10 (2004), 2682–2692
20. Gifford, A.N., Bruneus, M., Gatley, S.J., Volkow, N.D., Cannabinoid receptor-mediated inhibition of acetylcholine release from hippocampal and cortical synaptosomes. Br J Pharmacol 131:3 (2000), 645–650
21. Gong, N., Li, Y., Cai, G.Q., Niu, R.F., Fang, Q., Wu, K., Chen, Z., Lin, L.N., Xu, L., Fei, J., Xu, T.L., GABA transporter-1 activity modulates hippocampal theta oscillation and theta burst stimulation-induced long-term potentiation. J Neurosci 29:50 (2009), 15836–15845
22. Harkany, T., Härtig, W., Berghuis, P., Dobszay, M.B., Zilberter, Y., Edwards, R.H., Mackie, K., Ernfors, P., Complementary distribution of type 1 cannabinoid receptors and vesicular glutamate transporter 3 in basal forebrain suggests input-specific retrograde signalling by cholinergic neurons. Eur J Neurosci 18:7 (2003), 1979–1992
23. Harkany, T., Dobszay, M.B., Cayetanot, F., Härtig, W., Siegemund, T., Aujard, F., Mackie, K., Redistribution of CB1 cannabinoid receptors during evolution of cholinergic basal forebrain territories and their cortical projection areas: a comparison between the gray mouse lemur (Microcebus murinus, primates) and rat. Neuroscience 135:2 (2005), 595–609
24. Heider, M., Schliebs, R., Roβner, S., Bigl, V., Basal forebrain cholinergic immunolesion by 192IgG-saporin: evidence for a presynaptic location of subpopulations of alpha 2- and beta-adrenergic as well as 5-HT2A receptors on cortical cholinergic terminals. Neurochem Res 22:8 (1997), 957–966
25. Herzog, E., Gilchrist, J., Gras, C., Muzerelle, A., Ravassard, P., Giros, B., Gaspar, P., El Mestikawy, S., Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 123:4 (2004), 983–1002
26. Jeong da, U., Oh, J.H., Lee, J.E., Lee, J., Cho, Z.H., Chang, J.W., Chang, W.S., Basal forebrain cholinergic deficits reduce glucose metabolism and function of cholinergic and GABAergic systems in the cingulate cortex. Yonsei Med J 57:1 (2016), 165–172
27. Jeong, D.U., Chang, W.S., Hwang, Y.S., Lee, D., Chang, J.W., Decrease of GABAergic markers and arc protein expression in the frontal cortex by intraventricular 192IgG-saporin. Dement Geriatr Cogn Disord 32:1 (2011), 70–78
28. Karnovsky, M.J., Roots, L., A “direct-coloring” thiocholine method for cholinesterases. J Histochem Cytochem 12 (1964), 219–221
29. Kash, S.F., Tecott, L.H., Hodge, C., Baekkeskov, S., Increased anxiety and altered responses to anxiolytics in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci U S A 96 (1999), 1698–1703
30. Kathmann, M., Weber, B., Zimmer, A., Schlicker, E., Enhanced acetylcholine release in the hippocampus of cannabinoid CB(1) receptor-deficient mice. Br J Pharmacol 132:6 (2001), 1169–1173
31. Katona, I., Sperlágh, B., Sík, A., Käfalvi, A., Vizi, E.S., Mackie, K., Freund, T.F., Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19:11 (1999), 4544–4558
32. Katona, I., Rancz, E.A., Acsady, L., Ledent, C., Mackie, K., Hajos, N., Freund, T.F., Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J Neurosci 21:23 (2001), 9506–9518
33. Katona, I., Urbán, G.M., Wallace, M., Ledent, C., Jung, K.M., Piomelli, D., Mackie, K., Freund, T.F., Molecular composition of the endocannabinoid system at glutamatergic synapses. J Neurosci 26:21 (2006), 5628–5637
34. Kawamura, Y., Fukaya, M., Maejima, T., Yoshida, T., Miura, E., Watanabe, M., Ohno-Shosaku, T., Kano, M., The CB1 cannabinoid receptor is the major cannabinoid receptor at excitatory presynaptic sites in the hippocampus and cerebellum. J Neurosci 26:11 (2006), 2991–3001
35. Kim, J.J., DeCola, J.P., Landeira-Fernandez, J., Fanselow, M.S., N-methyl-D-aspartate receptor antagonist APV blocks acquisition but not expression of fear conditioning. Behav Neurosci 105:1 (1991), 126–133
36. Kim, J., Isokawa, M., Ledent, C., Alger, B.E., Activation of muscarinic acetylcholine receptors enhances the release of endogenous cannabinoids in the hippocampus. J Neurosci 22:23 (2002), 10182–10191
37. Lanctôt, K.L., Herrmann, N., Mazzotta, P., Khan, L.R., Ingber, N., GABAergic function in Alzheimer's disease: evidence for dysfunction and potential as a therapeutic target for the treatment of behavioural and psychological symptoms of dementia. Can J Psychiatry 49:7 (2004), 439–453
38. Lazarova-Bakarova, M.B., Petkova, B.P., Todorov, I.K., Petkov, V.D., Memory impairment induced by combined disturbance of noradrenergic and dopaminergic neurotransmissions: effects of nootropic drugs. Acta Physiol Pharmacol Bulg 17:1 (1991), 29–34
39. Lee, J.E., Jeong da, U., Lee, J., Chang, W.S., Chang, J.W., The effect of nucleus basalis magnocellularis deep brain stimulation on memory function in a rat model of dementia. BMC Neurol, 12(16), 2016, 26
40. Lu, X.R., Ong, W.Y., Mackie, K., A light and electron microscopic study of the CB1 cannabinoid receptor in monkey basal forebrain. J Neurocytol 28:12 (1999), 1045–1051
41. Manuel, I., de San, González., Román, E., Giralt, M.T., Ferrer, I., Rodríguez-Puertas, R., Type-1 cannabinoid receptor activity during Alzheimer's disease progression. J Alzheimers Dis 42:3 (2014), 761–766
42. Marsicano, G., Goodenough, S., Monory, K., Hermann, H., Eder, M., Cannich, A., Azad, S.C., Cascio, M.G., Gutiérrez, S.O., van der Stelt, M., López-Rodriguez, M.L., Casanova, E., Schütz, G., Zieglgänsberger, W., Di Marzo, V., Behl, C., Lutz, B., CB1cannabinoid receptors and on-demand defense against excitotoxicity. Science 302 (2003), 84–88
43. Martin, H.G., Bernabeu, A., Lassalle, O., Bouille, C., Beurrier, C., Pelissier-Alicot, A.L., Manzoni, O.J., Endocannabinoids mediate muscarinic acetylcholine receptor-dependent long-term depression in the adult medial prefrontal cortex. Front Cell Neurosci, 9, 2015, 457
44. Mulder, J., Zilberter, M., Pasquaré, S.J., Alpár, A., Schulte, G., Ferreira, S.G., Köfalvi, A., Martín-Moreno, A.M., Keimpema, E., Tanila, H., Watanabe, M., Mackie, K., Hortobágyi, T., de Ceballos, M.L., Harkany, T., Molecular reorganization of endocannabinoid signalling in Alzheimer's disease. Brain 134:Pt 4 (2011), 1041–1060
45. Myhrer, T., Neurotransmitter systems involved in learning and memory in the rat: a meta-analysis based on studies of four behavioral tasks. Brain Res Rev 41:2–3 (2003), 268–287
46. Nyíri, G., Szabadits, E., Cserép, C., Mackie, K., Shigemoto, R., Freund, T.F., GABAB and CB1 cannabinoid receptor expression identifies two types of septal cholinergic neurons. Eur J Neurosci 21:11 (2005), 3034–3042
47. Ohno-Shosaku, T., Maejima, T., Kano, M., Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29:3 (2001), 729–738
48. Pascual, A.C., Martín-Moreno, A.M., Giusto, N.M., de Ceballos, M.L., Pasquaré, S.J., Normal aging in rats and pathological aging in human Alzheimer's disease decrease FAAH activity: modulation by cannabinoid agonists. Exp Gerontol 60 (2014), 92–99
49. Paxinos, G., Watson, C., The rat brain in stereotaxic coordinates. 5th ed., 2005, Elsevier Academic Press, San Diego
50. Perry, E.K., Gibson, P.H., Blessed, G., Perry, R.H., Tomlinson, B.E., Neurotransmitter enzyme abnormalities in senile dementia. Choline acetyltransferase and glutamic acid decarboxylase activities in necropsy brain tissue. J Neurol Sci 34:2 (1977), 247–265
51. Perry, E., Walker, M., Grace, J., Perry, R., Acetylcholine in mind: a neurotransmitter correlate of consciousness?. Trends Neurosci 22:6 (1999), 273–280
52. Revuelta, A.V., Cheney, D.L., Costa, E., Lander, N., Mechoulam, R., Reduction of hippocampal acetylcholine turnover in rats treated with (−)-delta 8-tetrahydrocannabinol and its 1′,2′-dimethyl-heptyl homolog. Brain Res 195:2 (1980), 445–452
53. Rodríguez-Puertas, R., Pascual, J., Vilaró, T., Pazos, A., Autoradiographic distribution of M1, M2, M3, and M4 muscarinic receptor subtypes in Alzheimer's disease. Synapse 26:4 (1997), 341–350
54. Roβner, S., Schliebs, R., Bigl, V., Ibotenic acid lesions of nucleus basalis magnocellularis differentially affects cholinergic, glutamatergic and GABAergic markers in cortical rat brain regions. Brain Res 668 (1994), 85–99
55. Roβner, S., Härtig, W., Schliebs, R., Brückner, G., Brauer, K., Perez-Polo, J.R., Wiley, R.G., Bigl, V., 192IgG-saporin immunotoxin-induced loss of cholinergic cells differentially activates microglia in rat basal forebrain nuclei. J Neurosci Res 41:3 (1995), 335–346
56. Roβner, S., Schliebs, R., Bigl, V., 192IgG-saporin-induced immunotoxic lesions of cholinergic basal forebrain system differentially affect glutamatergic and GABAergic markers in cortical rat brain regions. Brain Res 696:1–2 (1995), 165–176
57. Schliebs, R., Feist, T., Roβner, S., Bigl, V., Receptor function in cortical rat brain regions after lesion of the nucleus basalis. J Neural Transm 44 (1994), 195–208
58. Stella, N., Piomelli, D., Receptor-dependent formation of endogenous cannabinoids in cortical neurons. Eur J Pharmacol 425:3 (2001), 189–196
59. Torres, E.M., Perry, T.A., Blockland, A., Wilkinson, L.S., Wiley, R.G., Lappi, D.A., Dunnet, S.B., Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system. Neuroscience 63:1 (1994), 95–122
60. Tsou, K., Mackie, K., Sañudo-Peña, M.C., Walker, J.M., Cannabinoid CB1 receptors are localized primarily on cholecystokinin-containing GABAergic interneurons in the rat hippocampal formation. Neuroscience 93:3 (1999), 969–975
61. Tulving, E., Episodic memory: from mind to brain. Annu Rev Psychol 53 (2002), 1–25
62. Tzavara, E.T., Wade, M., Nomikos, G.G., Biphasic effects of cannabinoids on acetylcholine release in the hippocampus: site and mechanism of action. J Neurosci 23:28 (2003), 9374–9384
63. Varvel, S.A., Anum, E., Niyuhire, F., Wise, L.E., Lichtman, A.H., Delta(9)-THC-induced cognitive deficits in mice are reversed by the GABA(A) antagonist bicuculline. Psychopharmacology 178:2–3 (2005), 317–327
64. Venable, N., Kelly, P.H., Effects of NMDA receptor antagonists on passive avoidance learning and retrieval in rats and mice. Psychopharmacology 100:2 (1990), 215–221
65. Vierck, C.J., Yezierski, R.P., Wiley, R.G., Pain sensitivity following loss of cholinergic basal forebrain (CBF) neurons in the rat. Neuroscience 319 (2016), 23–34
66. Wenk, G.L., Stoehr, J.D., Quintana, G., Mobley, S., Wiley, R.G., Behavioral, biochemical, histological, and electrophysiological effects of 192IgG-saporin injections into the basal forebrain of rats. J Neurosci 14:10 (1994), 5986–5995
67. Westlake, T.M., Howlett, A.C., Bonner, T.I., Matsuda, L.A., Herkenham, M., Cannabinoid receptor binding and messenger RNA expression in human brain: an in vitro receptor autoradiography and in situ hybridization histochemistry study of normal aged and Alzheimer's brains. Neuroscience 63:3 (1994), 637–652
68. Whitehouse, P.J., Price, D.L., Struble, R.G., Clark, A.W., Coyle, J.T., Delon, M.R., Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 215:4537 (1982), 1237–1239
69. Yeh, M.L., Selvam, R., Levine, E.S., BDNF-induced endocannabinoid release modulates neocortical glutamatergic neurotransmission. Synapse, 71(5), 2017
70. Zhao, P., Leonoudakis, D., Abood, M.E., Beattie, E.C., Cannabinoid receptor activation reduces TNFalpha-induced surface localization of AMPAR-type glutamate receptors and excitotoxicity. Neuropharmacology 58:2 (2010), 551–558