Functional autoradiography shows unaltered cannabinoid CB1 receptor signalling in hippocampus and cortex of APP/PS1 transgenic mice

CNS and Neurological Disorders - Drug Targets

Volumn 11, Issue 8, 2012, Pages 1038-1044

  Karkkainen E ^a   Tanila, H ^a,b   Laitinen, J T ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

Alzheimer's disease; APPswe; Cannabinoid signalling; CB1 receptor; Endocannabinoid; PS1dE9

Indexed keywords

4 (1, 1 DIMETHYLHEPTYL) 1', 2', 3', 4', 5', 6' HEXAHYDRO 2, 3' DIHYDROXY 6' (3 HYDROXYPROPYL) BIPHENYL; CANNABINOID 1 RECEPTOR; DITHIOTHREITOL; GUANOSINE TRIPHOSPHATE; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; CONTROLLED STUDY; ENTORHINAL CORTEX; FEMALE; FRONTAL CORTEX; HIPPOCAMPUS; MOUSE; NONHUMAN; SUBSTANTIA NIGRA;

EID: 84875046157     PISSN: 18715273     EISSN: 19963181     Source Type: Journal    
DOI: 10.2174/1871527311211080014     Document Type: Article

References (55)

1. Selkoe, D.J. Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev., 2001, 81, 741-766.
2. Bartus, R.T.; Dean, R.L. 3rd; Beer, B.; Lippa, A.S. The cholinergic hypothesis of geriatric memory dysfunction. Science, 1982, 217(4558), 408-414.
3. Emre, M.; Genla, C.; Ransil, B.J.; Mesulam, M.M. The acute neurotoxicity and effects upon cholinergic axons of intracerebrally injected α-amyloid in the rat brain. Neurobiol. Aging, 1992, 13, 553-559.
4. (1-42)affects cholinergic but not parvalbumincontaining neurons in the septal complex of the rat. Brain Res., 1995, 698, 270-274.
5. 24)25-35 in rat nucleus basalis induces behavioral dysfunctions, impairs learning and memory and disrupts cortical cholinergic innervation. Behav. Brain Res., 1998, 90(2), 133-145.
6. Harkany, T.; Abrahám, I.; Timmerman, W.; Laskay, G.; Tóth, B.; Sasvári, M.; Kónya, C.; Sebens, J.B.; Korf, J.; Nyakas, C.; Zarándi, M.; Soós, K.; Penke, B.; Luiten, P.G. Beta-amyloid neurotoxicity is mediated by a glutamate-triggered excitotoxic cascade in rat nucleus basalis. Eur. J. Neurosci., 2000, 12(8), 2735-2745.
7. Lyness, S.A.; Zarow, C.; Chui, H.C. Neuron loss in key cholinergic and aminergic nuclei in Alzheimer disease: a meta-analysis. Neurobiol. Aging, 2003, 24, 1-23.
8. Palmer, A.M.; DeKosky, S.T. Monoamine neurons in aging and Alzheimer's disease. J. Neural Transm. Gen. Sect., 1993, 91(2-3), 135-159.
9. Parvizi, J.; Van Hoesen, G.W.; Damasio, A. The selective vulnerability of brainstem nuclei to Alzheimer's disease. Ann. Neurol., 2001, 49, 53-66.
10. Rub, U.; Del Tredici, K.; Schultz, C.; Thal, D.R.; Braak, E.; Braak, H. The evolution of Alzheimer's disease-related cytoskeletal pathology in the human raphe nuclei. Neuropathol. Appl. Neurobiol., 2000, 26, 553-567.
11. Zweig, R.M.; Ross, C.A.; Hedreen, J.C.; Steele, C.; Cardillo, J.E.; Whitehouse, P.J.; Folstein, M.F.; Price, D.L. The neuropathology of aminergic nuclei in Alzheimer's disease. Ann. Neurol., 1988, 24, 233-242.
12. Machová, E.; Jakubík, J.; Michal, P.; Oksman, M.; Iivonen, H.; Tanila, H.; Dolezal, V. Impairment of muscarinic transmission in transgenic APPswe/PS1dE9 mice. Neurobiol. Aging, 2008, 29(3), 368-378.
13. Wong, T.P.; Debeir, T.; Duff, K.; Cuello, A.C. Reorganization of cholinergic terminals in the cerebral cortex and hippocampus in transgenic mice carrying mutated presenilin-1 and amyloid precursor protein transgenes. J. Neurosci., 1999, 19(7), 2706-2716.
14. Liu, Y.; Yoo, M.J.; Savonenko, A.; Stirling, W.; Price, D.L.; Borchelt, D.R.; Mamounas, L.; Lyons, W.E.; Blue, M.E.; Lee, M.K. Amyloid pathology is associated with progressive monoaminergic neurodegeneration in a transgenic mouse model of Alzheimer's disease. J. Neurosci., 2008, 28(51), 13805-13814.
15. Perez, S.E.; Lazarov, O.; Koprich, J.B.; Chen, E.Y.; Rodriguez-Menendez, V.; Lipton, J.W.; Sisodia, S.S.; Mufson, E.J. Nigrostriatal dysfunction in familial Alzheimer's disease-linked APPswe/PS1DeltaE9 transgenic mice. J. Neurosci., 2005, 25(44), 10220-10229.
16. Piomelli, D. The molecular logic of endocannabinoid signalling. Nat. Rev. Neurosci., 2003, 4(11), 873-884.
17. Herkenham, M.; Lynn, A.B.; Little, M.D.; Johnson, M.R.; Melvin, L.S.; de Costa, B.R.; Rice, K.C. Cannabinoid receptor localization in brain. Proc. Natl. Acad. Sci. U. S. A., 1990, 87(5), 1932-1936.
18. Mechoulam, R.; Ben-Shabat, S.; Hanus, L.; Ligumsky, M.; Kaminski, N.E.; Schatz, A.R.; Gopher, A.; Almog, S.; Martin, B.R.; Compton, D.R.; Pertwee, R.G.; Griffin, G.; Bayewitch, M.; Barg, J.; Vogel, Z. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem. Pharmacol., 1995, 50(1), 83-90.
19. Devane, W.A.; Hanus, L.; Breuer, A.; Pertwee, R.G.; Stevenson, L.A.; Griffin, G.; Gibson, D.; Mandelbaum, A.; Etinger, A.; Mechoulam, R. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science, 1992, 258(5090), 1946-1949.
20. Eljaschewitsch, E.; Witting, A.; Mawrin, C.; Lee, T.; Schmidt, P.M.; Wolf, S.; Hoertnagl, H.; Raine, C.S.; Schneider-Stock, R.; Nitsch, R.; Ullrich, O. The endocannabinoid anandamide protects neurons during CNS inflammation by induction of MKP-1 in microglial cells. Neuron, 2006, 49(1), 67-79.
21. Kano, M.; Ohno-Shosaku, T.; Hashimotodani, Y.; Uchigashima, M.; Watanabe, M. Endocannabinoid-mediated control of synaptic transmission. Physiol. Rev., 2009, 89(1), 309-380.
22. Sugiura, T.; Kishimoto, S.; Oka, S.; Gokoh, M. Biochemistry, pharmacology and physiology of 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand. Prog. Lipid Res., 2006, 45(5), 405-446.
23. Carlson, G.; Wang, Y.; Alger, B.E. Endocannabinoids facilitate the induction of LTP in the hippocampus. Nat. Neurosci., 2002, 5, 723-724.
24. Marsicano, G.; Wotjak, C.T.; Azad, S.C.; Bisogno, T.; Rammes, G.; Cascio, M.G.; Hermann, H.; Tang, J.; Hofmann, C.; Zieglgänsberger, W.; Di Marzo, V.; Lutz, B. The endogenous cannabinoid system controls extinction of aversive memories. Nature, 2002, 418(6897), 530-534.
25. Martin, M.; Ledent, C.; Parmentier, M.; Maldonado, R.; Valverde, O. Involvement of CB1 cannabinoid receptors in emotional behaviour. Psychopharmacology (Berl.), 2002, 159, 379-387.
26. 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., 2011, 108(27), 11256-11261.
27. 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. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science, 2003, 302(5642), 84-88.
28. Alger, B.E. Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog. Neurobiol., 2002, 68(4), 247-86.
29. Savinainen, J.R.; Saario, S.M.; Laitinen, J.T. The serine hydrolases MAGL, ABHD6 and ABHD12 as guardians of 2-arachidonoylglycerol signalling through cannabinoid receptors. Acta. Physiol. (Oxf.), 2012, 204(2), 267-276.
30. 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, 1994, 63(3), 637-652.
31. Lee, J.H.; Agacinski, G.; Williams, J.H.; Wilcock, G.K.; Esiri, M.M.; Francis, P.T.; Wong, P.T.; Chen, C.P.; Lai, M.K. Intact cannabinoid CB1 receptors in the Alzheimeŕs disease cortex. Neurochem. Int., 2010, 57(8), 985-989.
32. 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, 2011, 134(Pt 4), 1041-1060.
33. Ramírez, B.G.; Blázquez, C.: Gómez del Pulgar, T.; Guzmán, M.; de Ceballos, M.L. Prevention of Alzheimeŕs disease pathology by cannabinoids: neuroprotection mediated by blockade of microglial activation. J. Neurosci., 2005, 25(8), 1904-1913.
34. Kalifa, S.; Polston, E.K.; Allard, J.S.; Manaye, K.F. Distribution Patterns of Cannabinoid CB1 receptors in the hippocampus of APP(swe)/PS1(αE9) double transgenic mice. Brain Res., 2011, 1376, 94-100.
35. ifamily of G proteins. Curr. Neuropharmacol., 2004, 2, 191-206.
36. Garcia-Alloza, M.; Robbins, E.M.; Zhang-Nunes, S.X.; Purcell, S.M.; Betensky, R.A.; Raju, S.; Prada, C.; Greenberg, S.M.; Bacskai, B.J.; Frosch, M.P. Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol. Dis., 2006, 24(3), 516-524.
37. Jankowsky, J.L.; Fadale, D.J.; Anderson, J.; Xu, G.M.; Gonzales, V.; Jenkins, N.A.; Copeland, N.G.; Lee, M.K.; Younkin, L.H.; Wagner, S.L.; Younkin, S.G.; Borchelt, D.R. Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum. Mol. Genet., 2004, 13, 159-170.
38. Minkeviciene, R.; Ihalainen, J.; Malm, T.; Matilainen, O.; Keksa-Goldsteine, V.; Goldsteins, G.; Iivonen, H.; Leguit, N.; Glennon, J.; Koistinaho, J.; Banerjee, P.; Tanila, H. Age-related decrease in stimulated glutamate release and vesicular glutamate transporters in APP/PS1 transgenic and wild-type mice. J. Neurochem., 2008, 105(3), 584-594.
39. sted.; Academic Press, Inc.: USA, 1997.
40. Palomäki, V.A.B.; Lehtonen, M.; Savinainen, J.R.; Laitinen, J.T. Visualization of 2-arachidonoylglycerol accumulation and cannabinoid CB1 receptor activity in rat brain cryosections by functional autoradiography. J. Neurochem., 2007, 101, 972-981.
41. Kokkola, T.; Savinainen, J.R.; Mönkkönen, K.S.; Durán Retamal, M.; Laitinen, J.T. S-Nitrosothiols modulate G protein-coupled receptor signaling in a reversible and highly receptor-specific manner. BMC Cell Biol., 2005, 6(1), 21.
42. Lewandowicz, A.M.; Vepsäläinen, J.; Laitinen, J.T. The "allosteric modulator" SCH-202676 disrupts G protein-coupled receptor function via sulfhydryl-sensitive mechanisms. Br. J. Pharmacol., 2006, 147, 422-429.
43. Herkenham, M.; Lynn, A.B.; Johnson, M.R.; Melvin, L.S.; de Costa, B.R.; Rice, K.C. Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J. Neurosci., 1991, 11(2), 563-583.
44. Chanda, P.K.; Gao, Y.; Mark, L.; Btesh, J.; Strassle, B.W.; Lu, P.; Piesla, M.J.; Zhang, M.Y.; Bingham, B.; Uveges, A.; Kowal, D.; Garbe, D.; Kouranova, E.V.; Ring, R.H.; Bates, B.; Pangalos, M.N.; Kennedy, J.D.; Whiteside, G.T.; Samad, T.A. Monoacylglycerol lipase activity is a critical modulator of the tone and integrity of the endocannabinoid system. Mol. Pharmacol., 2010, 78(6), 996-1003.
45. Schlosburg, J.E.; Blankman, J.L.; Long, J.Z.; Nomura, D.K.; Pan, B.; Kinsey, S.G.; Nguyen, P.T.; Ramesh, D.; Booker, L.; Burston, J.J.; Thomas, E.A.; Selley, D.E.; Sim-Selley, L.J.; Liu, Q.S.; Lichtman, A.H.; Cravatt, B.F. Chronic monoacylglycerol lipase blockade causes functional antagonism of the endocannabinoid system. Nat. Neurosci., 2010, 13(9), 1113-1119.
46. Taschler, U.; Radner, F.P.; Heier, C.; Schreiber, R.; Schweiger, M.; Schoiswohl, G.; Preiss-Landl, K.; Jaeger, D.; Reiter, B.; Koefeler, H.C.; Wojciechowski, J.; Theussl, C.; Penninger, J.M.; Lass, A.; Haemmerle, G.; Zechner, R.; Zimmermann, R. Monoglyceride lipase-deficiency in mice impairs lipolysis and attenuates dietinduced insulin resistance. J. Biol. Chem., 2011, 286(20), 17467-17477.
47. Braak, H.; Braak, E. Neuropathological staging of Alzheimerrelated changes. Acta Neuropathol., 1991, 82, 239-259.
48. Thal, D.R.; Rub, U.; Orantes, M.; Braak, H. Phases of A beta deposition in the human brain and its relevance for the development of AD. Neurology, 2002, 58, 1791-1800.
49. West, M.J.; Coleman, P.D.; Flood, D.G.; Troncoso, J.C. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet, 1994, 344(8925), 769-772.
50. Laakso, M.P.; Partanen, K.; Riekkinen, P.; Lehtovirta, M.; Helkala, E.L.; Hallikainen, M.; Hänninen, T.; Vainio, P.; Soininen, H. Hippocampal volumes in Alzheimer's disease, Parkinson's disease with and without dementia, and in vascular dementia: An MRI study. Neurology, 1996, 46(3), 678-681.
51. Kummer, M.P.; Hermes, M.; Delekarte, A.; Hammerschmidt, T.; Kumar, S.; Terwel, D.; Walter, J.; Pape, H.C.; König, S.; Roeber, S.; Jessen, F.; Klockgether, T.; Korte, M.; Heneka, M.T. Nitration of tyrosine 10 critically enhances amyloid β aggregation and plaque formation. Neuron, 2011, 71(5), 833-844.
52. Ruan, L.; Kang, Z.; Pei, G.; Le, Y. Amyloid deposition and inflammation in APPswe/PS1dE9 mouse model of Alzheimer's disease. Curr. Alzheimer Res., 2009, 6(6), 531-540.
53. Aizenstein, H.J.; Nebes, R.D.; Saxton, J.A.; Price, J.C.; Mathis, C.A.; Tsopelas, N.D.; Ziolko, S.K.; James, J.A.; Snitz, B.E.; Houck, P.R.; Bi, W.; Cohen, A.D.; Lopresti, B.J.; DeKosky, S.T.; Halligan, E.M.; Klunk, W.E. Frequent amyloid deposition without significant cognitive impairment among the elderly. Arch. Neurol., 2008, 65, 1509-1517.
54. Kadir, A.; Almkvist, O.; Forsberg, A.; Wall, A.; Engler, H.; Långström, B.; Nordberg, A. Dynamic changes in PET amyloid and FDG imaging at different stages of Alzheimer's disease. Neurobiol. Aging, 2010, 33(1):198. e1-14.
55. Ashe, K.H.; Zahs, K.R. Probing the biology of Alzheimer's disease in mice. Neuron, 2010, 66(5), 631-645.