Genetic deletion of CB1 cannabinoid receptors exacerbates the Alzheimer-like symptoms in a transgenic animal model

Biochemical Pharmacology

Volumn 157, Issue , 2018, Pages 210-216

  Aso, Ester ^a,b   Andrés Benito, Pol ^a,b   Ferrer, Isidre ^a,b  

^a UNIVERSITY OF BARCELONA   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

Alzheimer's disease; Amyloid; APP PS1 mice; Cannabinoid receptor 1; Cognitive impairment

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; CANNABINOID 1 RECEPTOR; DISKS LARGE HOMOLOG 4; NEURON SPECIFIC NUCLEAR PROTEIN; PARVALBUMIN; PRESENILIN 1; CNR1 PROTEIN, MOUSE; NERVE PROTEIN;

AGE; ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CONTROLLED STUDY; DEATH; DISEASE ASSOCIATION; DISEASE EXACERBATION; FEMALE; GENE DELETION; GENE EXPRESSION; HETEROZYGOTE; HIPPOCAMPUS; KNOCKOUT MOUSE; MALE; MEMORY DISORDER; MORTALITY; MOUSE; MUTANT; NERVE CELL; NEUROPATHOLOGY; NEUROTRANSMISSION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION LEVEL; SEIZURE; SURVIVAL; SYNAPTOGENESIS; TRANSGENE; TRANSGENIC MOUSE; ANIMAL; BRAIN; DISEASE MODEL; GENETICS; METABOLISM; PATHOLOGY; SURVIVAL ANALYSIS;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; MEMORY DISORDERS; MICE, KNOCKOUT; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; PRESENILIN-1; RECEPTOR, CANNABINOID, CB1; SURVIVAL ANALYSIS;

EID: 85051475597     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2018.08.007     Document Type: Article

References (39)

1. Amatniek, J.C., Hauser, W.A., DelCastillo-Castaneda, C., Jacobs, D.M., Marder, K., Bell, K., Albert, M., Brandt, J., Stern, Y., Incidence and predictors of seizures in patients with Alzheimer's disease. Epilepsia 47 (2006), 867–872.
2. Aso, E., Lomoio, S., López-González, I., Joda, L., Carmona, M., Fernández-Yagüe, N., Moreno, J., Juvés, S., Pujol, A., Pamplona, R., Portero-Otin, M., Martín, V., Díaz, M., Ferrer, I., Amyloid generation and dysfunctional immunoproteasome activation with disease progression in animal model of familial Alzheimer's disease. Brain Pathol. 22 (2012), 636–653.
3. 1 agonist ACEA protects neurons and reduces the cognitive impairment of AβPP/PS1 mice. J. Alzheimers Dis. 30 (2012), 439–459.
4. Aso, E., Sánchez-Pla, A., Vegas-Lozano, E., Maldonado, R., Ferrer, I., Cannabis-based medicine reduces multiple pathological processes in AβPP/PS1 mice. J. Alzheimers Dis. 43 (2015), 977–991.
5. 1 receptors. Proc. Natl. Acad. Sci. U.S.A. 102 (2005), 15670–15675.
6. Borchelt, D.R., Ratovitski, T., van Lare, J., Lee, M.K., Gonzales, V., Jenkins, N.A., Copeland, N.G., Price, D.L., Sisodia, S.S., Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 19 (1997), 939–945.
7. Chen, B., Bromley-Brits, K., He, G., Cai, F., Zhang, X., Song, W., Effect of synthetic cannabinoid HU210 on memory deficits and neuropathology in Alzheimer's disease mouse model. Curr. Alzheimer Res. 7 (2010), 255–261.
8. Chen, X., Zhang, J., Chen, C., Endocannabinoid 2-arachidonoylglycerol protects neurons against β-amyloid insults. Neuroscience 178 (2011), 159–168.
9. Chen, X., Nelson, C.D., Li, X., Winters, C.A., Azzam, R., Sousa, A.A., Leapman, R.D., Gainer, H., Sheng, M., Reese, T.S., PSD-95 is required to sustain the molecular organization of the postsynaptic density. J. Neurosci. 31 (2011), 6329–6338.
10. Chen, M., Wan, Y., Ade, K., Ting, J., Feng, G., Calakos, N., Sapap3 deletion anomalously activates short-term endocannabinoid-mediated synaptic plasticity. J. Neurosci. 31 (2011), 9563–9573.
11. Cloyd, J., Hauser, W., Towne, A., Ramsay, R., Mattson, R., Gilliam, F., Walczak, T., Epidemiological and medical aspects of epilepsy in the elderly. Epilepsy Res. 68:Suppl. 1 (2006), S39–S48.
12. Davies, P., Katzman, R., Terry, R.D., Reduced somatostatin–like immunoreactivity in cerebral cortex from cases of Alzheimer disease and Alzheimer senile dementia. Nature 288 (1980), 279–280.
13. Fagan, S.G., Campbell, V.A., The influence of cannabinoids on generic traits of neurodegeneration. Br. J. Pharmacol. 171 (2014), 1347–1360.
14. Ferrer, I., Defining Alzheimer as a common age-related neurodegenerative process not inevitably leading to dementia. Prog. Neurobiol. 97 (2012), 38–51.
15. 1 cannabinoid receptor activation rescues amyloid β-induced alterations in behaviour and intrinsic electrophysiological properties of rat hippocampal CA1 pyramidal neurones. Cell. Physiol. Biochem. 29 (2012), 391–406.
16. Howlett, A.C., Cannabinoid receptor signaling. Handb. Exp. Pharmacol. 168 (2005), 53–79.
17. Irizarry, M.C., Jin, S., He, F., Emond, J.A., Raman, R., Thomas, R.G., Sano, M., Quinn, J.F., Tariot, P.N., Galasko, D.R., Ishihara, L.S., Weil, J.G., Aisen, P.S., Incidence of new-onset seizures in mild to moderate Alzheimer disease. Arch. Neurol. 69 (2012), 368–372.
18. Janefjord, E., Mååg, J.L., Harvey, B.S., Smid, S.D., Cannabinoid Effects on β Amyloid Fibril and Aggregate Formation, Neuronal and Microglial-Activated Neurotoxicity In Vitro. Cell. Mol. Neurobiol. 34 (2014), 31–42.
19. 1 cannabinoid receptors in the hippocampus of APPswe/PS1ΔE9 double transgenic mice. Brain Res. 1376 (2011), 94–100.
20. Liu, J., Chang, L., Roselli, F., Almeida, O.F., Gao, X., Wang, X., Yew, D.T., Wu, Y., Amyloid-β induces caspase-dependent loss of PSD-95 and synaptophysin through NMDA receptors. J. Alzheimers Dis. 22 (2010), 541–556.
21. Lutz, B., On-demand activation of the endocannabinoid system in the control of neuronal excitability and epileptiform seizures. Biochem. Pharmacol. 68 (2004), 1691–1698.
22. Maccarrone, M., Totaro, A., Leuti, A., Giacovazzo, G., Scipioni, L., Mango, D., Coccurello, R., Nisticò R., Oddi, S., Early alteration of distribution and activity of hippocampal type-1 cannabinoid receptor in Alzheimer's disease-like mice overexpressing the human mutant amyloid precursor protein. Pharmacol. Res. 130 (2018), 366–373.
23. 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 (2014), 761–766.
24. 1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302 (2003), 84–88.
25. Mitew, S., Kirkcaldie, M.T., Dickson, T.C., Vickers, J.C., Altered synapses and gliotransmission in Alzheimer's disease and AD model mice. Neurobiol. Aging 34 (2013), 2341–2351.
26. Monory, K., Massa, F., Egertová M., Eder, M., Blaudzun, H., Westenbroek, R., Kelsch, W., Jacob, W., Marsch, R., Ekker, M., Long, J., Rubenstein, J.L., Goebbels, S., Nave, K.A., During, M., Klugmann, M., Wölfel, B., Dodt, H.U., Zieglgänsberger, W., Wotjak, C.T., Mackie, K., Elphick, M.R., Marsicano, G., Lutz, B., The endocannabinoid system controls key epileptogenic circuits in the hippocampus. Neuron 51 (2006), 455–466.
27. Noonan, J., Tanveer, R., Klompas, A., Gowran, A., McKiernan, J., Campbell, V.A., Endocannabinoids prevent beta-amyloid-mediated lysosomal destabilization in cultured neurons. J. Biol. Chem. 285 (2010), 38543–38554.
28. Oyelami, T., Bondt, A., den Wyngaert, I.V., Hoorde, K.V., Hoskens, L., Shaban, H., Kemp, J.A., Drinkenburg, W.H., Age-dependent concomitant changes in synaptic dysfunction and GABAergic pathway in the APP/PS1 mouse model. Acta Neurobiol. Exp. (Wars) 76 (2016), 282–293.
29. Palop, J.J., Chin, J., Roberson, E.D., Wang, J., Thwin, M.T., Bien-Ly, N., Yoo, J., Ho, K.O., Yu, G.Q., Kreitzer, A., Finkbeiner, S., Noebels, J.L., Mucke, L., Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 55 (2007), 697–711.
30. Ramírez, B.G., Blázquez, C., Gómez del Pulgar, T., Guzmán, M., de Ceballos, M.L., Prevention of Alzheimer's disease pathology by cannabinoids: neuroprotection mediated by blockade of microglial activation. J. Neurosci. 25 (2005), 1904–1913.
31. Ramos, B., Baglietto-Vargas, D., del Río, J.C., Moreno-González, I., Santa-María, C., Jiménez, S., Caballero, C., López-Téllez, J.F., Khan, Z.U., Ruano, D., Gutiérrez, A., Vitorica, J., Early neuropathology of somatostatin/NPY GABAergic cells in the hippocampus of a PS1xAPP transgenic model of Alzheimer's disease. Neurobiol. Aging 27 (2006), 1658–1672.
32. 2 receptor and amyloid pathology in frontal cortex of Alzheimer's disease patients. Neurobiol. Aging 34 (2013), 805–808.
33. Selkoe, D.J., Preventing Alzheimer's disease. Science 337 (2012), 1488–1492.
34. Stumm, C., Hiebel, C., Hanstein, R., Purrio, M., Nagel, H., Conrad, A., Lutz, B., Behl, C., Clement, A.B., Cannabinoid receptor 1 deficiency in a mouse model of Alzheimer's disease leads to enhanced cognitive impairment despite of a reduction in amyloid deposition. Neurobiol. Aging 34 (2013), 2574–2584.
35. Takahashi, H., Brasnjevic, I., Rutten, B.P., Van Der Kolk, N., Perl, D.P., Bouras, C., Steinbusch, H.W., Schmitz, C., Hof, P.R., Dickstein, D.L., Hippocampal interneuron loss in an APP/PS1 double mutant mouse and in Alzheimer's disease. Brain Struct. Funct. 214 (2010), 145–160.
36. Verret, L., Mann, E.O., Hang, G.B., Barth, A.M., Cobos, I., Ho, K., Devidze, N., Masliah, E., Kreitzer, A.C., Mody, I., Mucke, L., Palop, J.J., Inhibitory interneuron deficit links altered network activity and cognitive dysfunction in Alzheimer model. Cell 149 (2012), 708–721.
37. Walsh, D.M., Selkoe, D.J., Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 44 (2004), 181–193.
38. Woo, J.A., Boggess, T., Uhlar, C., Wang, X., Khan, H., Cappos, G., Joly-Amado, A., De Narvaez, E., Majid, S., Minamide, L.S., Bamburg, J.R., Morgan, D., Weeber, E., Kang, D.E., RanBP9 at the intersection between cofilin and Aβ pathologies: rescue of neurodegenerative changes by RanBP9 reduction. Cell Death Dis., 6, 2015, 1676.
39. 1 receptor knockout mice. Proc. Natl. Acad. Sci. U.S.A. 96 (1999), 5780–5785.