Alleviation of Neuropathology by Inhibition of Monoacylglycerol Lipase in APP Transgenic Mice Lacking CB2 Receptors

Molecular Neurobiology

Volumn 55, Issue 6, 2018, Pages 4802-4810

  Zhang, Jian ^a   Chen, Chu ^a,b  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

2 Arachidonoylglycerol, monoacylglycerol lipase; Cannabinoid receptor; Cyclooxygenase, arachidonic acid, prostaglandin; Endocannabinoid

Indexed keywords

4 [BIS(1,3 BENZODIOXOL 5 YL)HYDROXYMETHYL] 1 PIPERIDINECARBOXYLIC ACID 4 NITROPHENYL ESTER; ACYLGLYCEROL LIPASE; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; BETA SECRETASE; CANNABINOID 2 RECEPTOR; 1,3 BENZODIOXOLE DERIVATIVE; AMYLOID PRECURSOR PROTEIN; ASPARTIC PROTEINASE; BACE1 PROTEIN, MOUSE; PIPERIDINE DERIVATIVE; SECRETASE;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME INACTIVATION; ENZYME INHIBITION; FEMALE; MOUSE; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; TREATMENT DURATION; ANIMAL; ANTAGONISTS AND INHIBITORS; ASTROCYTE; BRAIN; COGNITION; DISEASE MODEL; DRUG EFFECT; GENETICS; METABOLISM; PATHOLOGY; SPATIAL LEARNING; TRANSGENIC MOUSE;

AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ACID ENDOPEPTIDASES; ASTROCYTES; BENZODIOXOLES; BRAIN; COGNITION; DISEASE MODELS, ANIMAL; MICE; MICE, TRANSGENIC; MONOACYLGLYCEROL LIPASES; NERVE DEGENERATION; PIPERIDINES; RECEPTOR, CANNABINOID, CB2; SPATIAL LEARNING;

EID: 85025471275     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-017-0689-x     Document Type: Article

References (47)

1. Chen X, Zhang J, Chen C (2011) Endocannabinoid 2-arachidonoylglycerol protects neurons against beta-amyloid insults. Neuroscience 178:159–168. doi:10.1016/j.neuroscience.2011.01.024
2. Du H, Chen X, Zhang J, Chen C (2011) Inhibition of COX-2 expression by endocannabinoid 2-arachidonoylglycerol is mediated via PPAR-gamma. Br J Pharmacol 163:1533–1549. doi:10.1111/j.1476-5381.2011.01444.x
3. Zhang J, Chen C (2008) Endocannabinoid 2-arachidonoylglycerol protects neurons by limiting COX-2 elevation. J Biol Chem 283:22601–22611. doi:10.1074/jbc.M800524200
4. Xu JY, Chen C (2015) Endocannabinoids in synaptic plasticity and neuroprotection. Neuroscientist 21:152–168. doi:10.1177/1073858414524632
5. Shohami E, Cohen-Yeshurun A, Magid L, Algali M, Mechoulam R (2011) Endocannabinoids and traumatic brain injury. Br J Pharmacol 163:1402–1410. doi:10.1111/j.1476-5381.2011.01343.x
6. Sugiura T, Kishimoto S, Oka S, Gokoh M (2006) Biochemistry, pharmacology and physiology of 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand. Prog Lipid Res 45:405–446. doi:10.1016/j.plipres.2006.03.003
7. Hermanson DJ, Gamble-George JC, Marnett LJ, Patel S (2014) Substrate-selective COX-2 inhibition as a novel strategy for therapeutic endocannabinoid augmentation. Trends Pharmacol Sci 35:358–367. doi:10.1016/j.tips.2014.04.006
8. Blankman JL, Simon GM, Cravatt BF (2007) A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol. Chem Biol 14:1347–1356. doi:10.1016/j.chembiol.2007.11.006
9. Nomura DK, Morrison BE, Blankman JL, Long JZ, Kinsey SG, Marcondes MC, Ward AM, Hahn YK et al (2011) Endocannabinoid hydrolysis generates brain prostaglandins that promote neuroinflammation. Science 334:809–813. doi:10.1126/science.1209200
10. Hein AM, O'Banion MK (2009) Neuroinflammation and memory: the role of prostaglandins. Mol Neurobiol 40:15–32. doi:10.1007/s12035-009-8066-z
11. Salmon JA, Higgs GA (1987) Prostaglandins and leukotrienes as inflammatory mediators. Br Med Bull 43:285–296
12. Chen C (2016) Endocannabinoid metabolism in neurodegenerative diseases. Neuroimmunol Neuroinflamm 3:268–270. doi:10.20517/2347-8659.2016.46
13. Chen R, Zhang J, Wu Y, Wang D, Feng G, Tang YP, Teng Z, Chen C (2012) Monoacylglycerol lipase is a therapeutic target for Alzheimer’s disease. Cell Rep 2:1329–1339. doi:10.1016/j.celrep.2012.09.030
14. Piro JR, Benjamin DI, Duerr JM, Pi Y, Gonzales C, Wood KM, Schwartz JW, Nomura DK et al (2012) A dysregulated endocannabinoid-eicosanoid network supports pathogenesis in a mouse model of Alzheimer’s disease. Cell Rep 1:617–623. doi:10.1016/j.celrep.2012.05.001
15. Atwood BK, Straiker A, Mackie K (2012) CB(2): therapeutic target-in-waiting. Prog Neuro-Psychopharmacol Biol Psychiatry 38:16–20. doi:10.1016/j.pnpbp.2011.12.001
16. Ashton JC, Glass M (2007) The cannabinoid CB2 receptor as a target for inflammation-dependent neurodegeneration. Curr Neuropharmacol 5:73–80
17. Cassano T, Calcagnini S, Pace L, De Marco F, Romano A, Gaetani S (2017) Cannabinoid receptor 2 signaling in neurodegenerative disorders: from pathogenesis to a promising therapeutic target. Front Neurosci 11:30. doi:10.3389/fnins.2017.00030
18. Brusco A, Tagliaferro P, Saez T, Onaivi ES (2008) Postsynaptic localization of CB2 cannabinoid receptors in the rat hippocampus. Synapse 62:944–949. doi:10.1002/syn.20569
19. den Boon FS, Chameau P, Schaafsma-Zhao Q, van Aken W, Bari M, Oddi S, Kruse CG, Maccarrone M et al (2012) Excitability of prefrontal cortical pyramidal neurons is modulated by activation of intracellular type-2 cannabinoid receptors. Proc Natl Acad Sci U S A 109:3534–3539. doi:10.1073/pnas.1118167109
20. Gong JP, Onaivi ES, Ishiguro H, Liu QR, Tagliaferro PA, Brusco A, Uhl GR (2006) Cannabinoid CB2 receptors: Immunohistochemical localization in rat brain. Brain Res 1071:10–23. doi:10.1016/j.brainres.2005.11.035
21. Li Y, Kim J (2015) Neuronal expression of CB2 cannabinoid receptor mRNAs in the mouse hippocampus. Neuroscience 311:253–267. doi:10.1016/j.neuroscience.2015.10.041
22. Stempel AV, Stumpf A, Zhang HY, Ozdogan T, Pannasch U, Theis AK, Otte DM, Wojtalla A et al (2016) Cannabinoid type 2 receptors mediate a cell type-specific plasticity in the hippocampus. Neuron 90:795–809. doi:10.1016/j.neuron.2016.03.034
23. Van Sickle MD, Duncan M, Kingsley PJ, Mouihate A, Urbani P, Mackie K, Stella N, Makriyannis A et al (2005) Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science 310:329–332. doi:10.1126/science.1115740
24. Zhang HY, Gao M, Liu QR, Bi GH, Li X, Yang HJ, Gardner EL, Wu J et al (2014) Cannabinoid CB2 receptors modulate midbrain dopamine neuronal activity and dopamine-related behavior in mice. Proc Natl Acad Sci U S A 111:E5007–E5015. doi:10.1073/pnas.1413210111
25. Ramirez BG, Blazquez C, Gomez del Pulgar T, Guzman M, de Ceballos ML (2005) Prevention of Alzheimer’s disease pathology by cannabinoids: neuroprotection mediated by blockade of microglial activation. J Neurosci 25:1904–1913. doi:10.1523/jneurosci.4540-04.2005
26. Solas M, Francis PT, Franco R, Ramirez MJ (2013) CB2 receptor and amyloid pathology in frontal cortex of Alzheimer’s disease patients. Neurobiol Aging 34:805–808. doi:10.1016/j.neurobiolaging.2012.06.005
27. Aso E, Andres-Benito P, Carmona M, Maldonado R, Ferrer I (2016) Cannabinoid receptor 2 participates in amyloid-beta processing in a mouse model of Alzheimer’s disease but plays a minor role in the therapeutic properties of a cannabis-based medicine. J Alzheimers Dis 51:489–500. doi:10.3233/jad-150913
28. Koppel J, Vingtdeux V, Marambaud P, d'Abramo C, Jimenez H, Stauber M, Friedman R, Davies P (2014) CB2 receptor deficiency increases amyloid pathology and alters tau processing in a transgenic mouse model of Alzheimer’s disease. Mol Med 20:29–36. doi:10.2119/molmed.2013.00140.revised
29. Schmole AC, Lundt R, Ternes S, Albayram O, Ulas T, Schultze JL, Bano D, Nicotera P et al (2015) Cannabinoid receptor 2 deficiency results in reduced neuroinflammation in an Alzheimer’s disease mouse model. Neurobiol Aging 36:710–719. doi:10.1016/j.neurobiolaging.2014.09.019
30. Aso E, Ferrer I (2016) CB2 cannabinoid receptor as potential target against Alzheimer’s disease. Front Neurosci 10:243. doi:10.3389/fnins.2016.00243
31. Zhang J, Hu M, Teng Z, Tang YP, Chen C (2014) Synaptic and cognitive improvements by inhibition of 2-AG metabolism are through upregulation of microRNA-188-3p in a mouse model of Alzheimer’s disease. J Neurosci 34:14919–14933. doi:10.1523/jneurosci.1165-14.2014
32. Pihlaja R, Takkinen J, Eskola O, Vasara J, Lopez-Picon FR, Haaparanta-Solin M, Rinne JO (2015) Monoacylglycerol lipase inhibitor JZL184 reduces neuroinflammatory response in APdE9 mice and in adult mouse glial cells. J Neuroinflammation 12:81. doi:10.1186/s12974-015-0305-9
33. Bisogno T, Oddi S, Piccoli A, Fazio D, Maccarrone M (2016) Type-2 cannabinoid receptors in neurodegeneration. Pharmacol Res 111:721–730. doi:10.1016/j.phrs.2016.07.021
34. Pan B, Wang W, Zhong P, Blankman JL, Cravatt BF, Liu QS (2011) Alterations of endocannabinoid signaling, synaptic plasticity, learning, and memory in monoacylglycerol lipase knock-out mice. J Neurosci 31:13420–13430. doi:10.1523/jneurosci.2075-11.2011
35. Selkoe DJ (2002) Alzheimer’s disease is a synaptic failure. Science 298:789–791. doi:10.1126/science.1074069
36. Long JZ, Li W, Booker L, Burston JJ, Kinsey SG, Schlosburg JE, Pavon FJ, Serrano AM et al (2009) Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects. Nat Chem Biol 5:37–44. doi:10.1038/nchembio.129
37. Long JZ, Nomura DK, Cravatt BF (2009) Characterization of monoacylglycerol lipase inhibition reveals differences in central and peripheral endocannabinoid metabolism. Chem Biol 16:744–753. doi:10.1016/j.chembiol.2009.05.009
38. Panikashvili D, Simeonidou C, Ben-Shabat S, Hanus L, Breuer A, Mechoulam R, Shohami E (2001) An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature 413:527–531. doi:10.1038/35097089
39. Chen C (2015) Homeostatic regulation of brain functions by endocannabinoid signaling. Neural Regen Res 10:691–692. doi:10.4103/1673-5374.156947
40. Song Y, Zhang J, Chen C (2015) Fine-tuning of synaptic upscaling at excitatory synapses by endocannabinoid signaling is mediated via the CB1 receptor. Sci Rep 5:16257. doi:10.1038/srep16257
41. Marchalant Y, Brothers HM, Norman GJ, Karelina K, DeVries AC, Wenk GL (2009) Cannabinoids attenuate the effects of aging upon neuroinflammation and neurogenesis. Neurobiol Dis 34:300–307
42. Petrosino S, Schiano Moriello A, Cerrato S, Fusco M, Puigdemont A, De Petrocellis L, Di Marzo V (2016) The anti-inflammatory mediator palmitoylethanolamide enhances the levels of 2-arachidonoyl-glycerol and potentiates its actions at TRPV1 cation channels. Br J Pharmacol 173:1154–1162. doi:10.1111/bph.13084
43. O'Sullivan SE (2016) An update on PPAR activation by cannabinoids. Br J Pharmacol 173:1899–1910. doi:10.1111/bph.13497
44. Bensinger SJ, Tontonoz P (2008) Integration of metabolism and inflammation by lipid-activated nuclear receptors. Nature 454:470–477. doi:10.1038/nature07202
45. Rockwell CE, Snider NT, Thompson JT, Vanden Heuvel JP, Kaminski NE (2006) Interleukin-2 suppression by 2-arachidonyl glycerol is mediated through peroxisome proliferator-activated receptor gamma independently of cannabinoid receptors 1 and 2. Mol Pharmacol 70:101–111. doi:10.1124/mol.105.019117
46. Chen R, Zhang J, Fan N, Teng ZQ, Wu Y, Yang H, Tang YP, Sun H et al (2013) Delta9-THC-caused synaptic and memory impairments are mediated through COX-2 signaling. Cell 155:1154–1165. doi:10.1016/j.cell.2013.10.042
47. Zhang J, Teng Z, Song Y, Hu M, Chen C (2015) Inhibition of monoacylglycerol lipase prevents chronic traumatic encephalopathy-like neuropathology in a mouse model of repetitive mild closed head injury. J Cereb Blood Flow Metab 35:443–453. doi:10.1038/jcbfm.2014.216