Inhibition of monoacylglycerol lipase prevents chronic traumatic encephalopathy-like neuropathology in a mouse model of repetitive mild closed head injury

Journal of Perinatology

Volumn 35, Issue 3, 2015, Pages 443-453

  Zhang, Jian ^a   Teng, Zhaoqian ^a   Song, Yunping ^a   Hu, Mei ^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; Alzheimer's disease; chronic traumatic encephalopathy; monoacylglycerol lipase; neurodegeneration; trauma brain injury

Indexed keywords

2-ARACHIDONYLGLYCEROL; ACYLGLYCEROL; ACYLGLYCEROL LIPASE; ARACHIDONIC ACID DERIVATIVE; ENDOCANNABINOID; 2 ARACHIDONOYLGLYCEROL; 4 [BIS(1,3 BENZODIOXOL 5 YL)HYDROXYMETHYL] 1 PIPERIDINECARBOXYLIC ACID 4 NITROPHENYL ESTER; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; GLUTAMATE RECEPTOR; INTERLEUKIN 1BETA; INTERLEUKIN 6; PROTEIN P25; PROTEIN P35; TAR DNA BINDING PROTEIN; TAU PROTEIN; TUMOR NECROSIS FACTOR ALPHA; VIMENTIN;

ANIMAL; BRAIN INJURY; C57BL MOUSE; COMPLICATION; DISEASE MODEL; HEAD INJURY; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; MOUSE; ORGAN CULTURE TECHNIQUE; PATCH CLAMP TECHNIQUE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; CHRONIC TRAUMATIC ENCEPHALOPATHY; COGNITION; CONTROLLED STUDY; CONVALESCENCE; CYTOKINE RELEASE; DEGENERATIVE DISEASE; ENZYME INACTIVATION; ENZYME INHIBITION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; MEMORY; NERVE CELL PLASTICITY; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SPATIAL LEARNING; SYNAPSE; SYNAPTIC TRANSMISSION; TRAUMATIC BRAIN INJURY;

ANIMALS; ARACHIDONIC ACIDS; BLOTTING, WESTERN; BRAIN INJURY, CHRONIC; DISEASE MODELS, ANIMAL; ENDOCANNABINOIDS; GLYCERIDES; HEAD INJURIES, CLOSED; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MONOACYLGLYCEROL LIPASES; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84938510532     PISSN: 07438346     EISSN: 14765543     Source Type: Journal    
DOI: 10.1038/jcbfm.2014.216     Document Type: Article

References (40)

1. Blennow K, Hardy J, Zetterberg H. The neuropathology and neurobiology of traumatic brain injury. Neuron 2012; 76: 886-899.
2. Goldstein LE, Fisher AM, Tagge CA, Zhang XL, Velisek L, Sullivan JA et al. Chronic traumatic encephalopathy in blast-exposed military veterans and a blast neurotrauma mouse model. Sci Transl Med 2012; 4: 134ra60.
3. Omalu B. Chronic traumatic encephalopathy. Progr Neurol Surg 2014; 28: 38-49.
4. Smith DH, Johnson VE, Stewart W. Chronic neuropathologies of single and repetitive TBI: substrates of dementia? Nat Rev Neurol 2013; 9: 211-221.
5. Creeley CE, Wozniak DF, Bayly PV, Olney JW, Lewis LM. Multiple episodes of mild traumatic brain injury result in impaired cognitive performance in mice. Acad Emerg Med 2004; 11: 809-819.
6. DeKosky ST, Blennow K, Ikonomovic MD, Gandy S. Acute and chronic traumatic encephalopathies: pathogenesis and biomarkers. Nature Rev Neurol 2013; 9: 192-200.
7. McKee AC, Robinson ME. Military-related traumatic brain injury and neurodegeneration. Alzheimer's Dementia 2014; 10: S242-S253.
8. McKee AC, Stern RA, Nowinski CJ, Stein TD, Alvarez VE, Daneshvar DH et al. The spectrum of disease in chronic traumatic encephalopathy. Brain 2013; 136: 43-64.
9. Jordan BD. The clinical spectrum of sport-related traumatic brain injury. Nat Rev Neurol 2013; 9: 222-230.
10. Lakis N, Corona RJ, Toshkezi G, Chin LS. Chronic traumatic encephalopathy-neuropathology in athletes and war veterans. Neurol Res 2013; 35: 290-299.
11. Stern RA, Riley DO, Daneshvar DH, Nowinski CJ, Cantu RC, McKee AC. Long-term consequences of repetitive brain trauma: chronic traumatic encephalopathy. PM & R 2011; 3: S460-S467.
12. Zetterberg H, Smith DH, Blennow K. Biomarkers of mild traumatic brain injury in cerebrospinal fluid and blood. Nat Rev Neurol 2013; 9: 201-210.
13. Woodcock T, Morganti-Kossmann MC. The role of markers of inflammation in traumatic brain injury. Front Neurol 2013; 4: 18.
14. Blankman JL, Simon GM, Cravatt BF. A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-Arachidonoylglycerol. Chem Biol 2007; 14: 1347-1356.
15. Long JZ, Nomura DK, Cravatt BF. Characterization of monoacylglycerol lipase inhibition reveals differences in central and peripheral endocannabinoid metabolism. Chem Biol 2009; 16: 744-753.
16. Panikashvili D, Mechoulam R, Beni SM, Alexandrovich A, Shohami E. CB1 cannabinoid receptors are involved in neuroprotection via NF-kappa B inhibition. J Cerebr Blood Flow Metab 2005; 25: 477-484.
17. Panikashvili D, Shein NA, Mechoulam R, Trembovler V, Kohen R, Alexandrovich A et al. The endocannabinoid 2-AG protects the blood-brain barrier after closed head injury and inhibits mRNA expression of proinflammatory cytokines. Neurobiol Dis 2006; 22: 257-264.
18. Panikashvili D, Simeonidou C, Ben-Shabat S, Hanus L, Breuer A, Mechoulam R et al. An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature 2001; 413: 527-531.
19. Chen R, Zhang J, Wu Y, Wang D, Feng G, Tang YP et al. Monoacylglycerol lipase is a therapeutic target for Alzheimer's disease. Cell Rep 2012; 2: 1329-1339.
20. Zhang J, Chen C. Endocannabinoid 2-Arachidonoylglycerol protects neurons by limiting COX-2 elevation. J Biol Chem 2008; 283: 22601-22611.
21. Nomura DK, Morrison BE, Blankman JL, Long JZ, Kinsey SG, Marcondes MC et al. Endocannabinoid hydrolysis generates brain prostaglandins that promote neuroinflammation. Science 2011; 334: 809-813.
22. Shohami E, Cohen-Yeshurun A, Magid L, Algali M, Mechoulam R. Endocannabinoids and traumatic brain injury. Br J Pharmacol 2011; 163: 1402-1410.
23. Luo J, Nguyen A, Villeda S, Zhang H, Ding Z, Lindsey D et al. Long-term cognitive impairments and pathological alterations in a mouse model of repetitive mild traumatic brain injury. Front Neurol 2014; 5: 12.
24. Meehan WP 3rd, Zhang J, Mannix R, Whalen MJ. Increasing recovery time between injuries improves cognitive outcome after repetitive mild concussive brain injuries in mice. Neurosurgery 2012; 71: 885-891.
25. Chen R, Zhang J, Fan N, Teng ZQ, Wu Y, Yang H et al. Delta9-THC-caused synaptic and memory impairments are mediated through COX-2 signaling. Cell 2013; 155: 1154-1165.
26. Flierl MA, Stahel PF, Beauchamp KM, Morgan SJ, Smith WR, Shohami E. Mouse closed head injury model induced by a weight-Drop device. Nature Protoc 2009; 4: 1328-1337.
27. Piro JR, Benjamin DI, Duerr JM, Pi Y, Gonzales C, Wood KM et al. A dysregulated endocannabinoid-eicosanoid network supports pathogenesis in a mouse model of Alzheimer's disease. Cell Rep 2012; 1: 617-623.
28. Levin HS, Robertson CS. Mild traumatic brain injury in translation. J Neurotrauma 2013; 30: 610-617.
29. Stein TD, Alvarez VE, McKee AC. Chronic traumatic encephalopathy: a spectrum of neuropathological changes following repetitive brain trauma in athletes and military personnel. Alzheimer's Res Ther 2014; 6: 4.
30. Klemenhagen KC, O'Brien SP, Brody DL. Repetitive concussive traumatic brain injury interacts with post-injury foot shock stress to worsen social and depressionlike behavior in mice. PloS One 2013; 8: e74510.
31. Mouzon B, Chaytow H, Crynen G, Bachmeier C, Stewart J, Mullan M et al. Repetitive mild traumatic brain injury in a mouse model produces learning and memory deficits accompanied by histological changes. J Neurotrauma 2012; 29: 2761-2773.
32. Mouzon BC, Bachmeier C, Ferro A, Ojo JO, Crynen G, Acker CM et al. Chronic neuropathological and neurobehavioral changes in a repetitive mild traumatic brain injury model. Ann Neurol 2014; 75: 241-254.
33. Petraglia AL, Plog BA, Dayawansa S, Chen M, Dashnaw ML, Czerniecka K et al. The spectrum of neurobehavioral sequelae after repetitive mild traumatic brain injury: a novel mouse model of chronic traumatic encephalopathy. J Neurotrauma 2014; 31: 1211-1224.
34. Shitaka Y, Tran HT, Bennett RE, Sanchez L, Levy MA, Dikranian K et al. Repetitive closed-skull traumatic brain injury in mice causes persistent multifocal axonal injury and microglial reactivity. J Neuropathol Exp Neurol 2011; 70: 551-567.
35. Yoshiyama Y, Uryu K, Higuchi M, Longhi L, Hoover R, Fujimoto S et al. Enhanced neurofibrillary tangle formation, cerebral atrophy, and cognitive deficits induced by repetitive mild brain injury in a transgenic tauopathy mouse model. J Neurotrauma 2005; 22: 1134-1141.
36. Kane MJ, Angoa-Perez M, Briggs DI, Viano DC, Kreipke CW, Kuhn DM. A mouse model of human repetitive mild traumatic brain injury. J Neurosci Methods 2012; 203: 41-49.
37. Mannix R, Meehan WP, Mandeville J, Grant PE, Gray T, Berglass J et al. Clinical correlates in an experimental model of repetitive mild brain injury. Ann Neurol 2013; 74: 65-75.
38. Xu JY, Chen C. Endocannabinoids in synaptic plasticity and neuroprotection. Neuroscientist advance online publication, 25 February 2014; doi: 10.1177/1073858414524632 (e-pub ahead of print).
39. Tchantchou F, Zhang Y. Selective inhibition of alpha/beta-hydrolase domain 6 attenuates neurodegeneration, alleviates blood brain barrier breakdown, and improves functional recovery in a mouse model of traumatic brain injury. J Neurotrauma 2013; 30: 565-579.
40. Zhang J, Hu M, Teng Z, Tang Y, Chen C. 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 2014; 34: 14919-14933.