Upregulation of the cannabinoid CB 2 receptor in environmental and viral inflammation-driven rat models of Parkinson's disease

Experimental Neurology

Volumn 283, Issue , 2016, Pages 204-212

  Concannon, Ruth M ^a   Okine, Bright N ^a   Finn, David P ^a   Dowd, Eilís ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

CB 2 receptors; Endocannabinoid system; Microglia; Neuroinflammation; Parkinson's disease

Indexed keywords

CANNABINOID 2 RECEPTOR; ENDOCANNABINOID; POLYINOSINIC POLYCYTIDYLIC ACID; ROTENONE; CD11B ANTIGEN; CNR2 PROTEIN, RAT; INSECTICIDE; MESSENGER RNA;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; ENVIRONMENTAL FACTOR; IMMUNOHISTOCHEMISTRY; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; MICROGLIA; MOTOR DYSFUNCTION; NERVE CELL; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; ANALYSIS OF VARIANCE; ANIMAL; DISEASE MODEL; DRUG EFFECT; ENVIRONMENT; GENETICS; HEMISPHERIC DOMINANCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; MOTOR ACTIVITY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; TANDEM MASS SPECTROMETRY; TIME FACTOR;

ANALYSIS OF VARIANCE; ANIMALS; CD11B ANTIGEN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DISEASE MODELS, ANIMAL; ENVIRONMENT; FUNCTIONAL LATERALITY; INSECTICIDES; MALE; MOTOR ACTIVITY; PARKINSON DISEASE; POLY I-C; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB2; RNA, MESSENGER; ROTENONE; TANDEM MASS SPECTROMETRY; TIME FACTORS; UP-REGULATION;

EID: 84975871967     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2016.06.014     Document Type: Article

References (57)

1. Atwood, B.K., Mackie, K., CB2: A cannabinoid receptor with an identity crisis. Br. J. Pharmacol. 160 (2010), 467–479.
2. 2 receptor. J. Neurosci. Methods, 2013.
3. 2 receptors and fatty acid amide hydrolase are selectively overexpressed in neuritic plaque-associated glia in Alzheimer's disease brains. J. Neurosci. 23 (2003), 11136–11141.
4. Benito, C., Romero, J.P., Tolón, R.M., Clemente, D., Docagne, F., Hillard, C.J., Guaza, C., Romero, J., Cannabinoid CB1 and CB2 receptors and fatty acid amide hydrolase are specific markers of plaque cell subtypes in human multiple sclerosis. J. Neurosci. 27 (2007), 2396–2402.
5. Bobyn, J., Mangano, E.N., Gandhi, A., Nelson, E., Moloney, K., Clarke, M., Hayley, S., Viral-toxin interactions and Parkinson's disease: poly (I: C) priming enhanced the neurodegenerative effects of paraquat. J. Neuroinflammation, 9, 2012, 86.
6. Burstein, S.H., Zurier, R.B., Cannabinoids, endocannabinoids, and related analogs in inflammation. AAPS J. 11 (2009), 109–119.
7. Concannon, R., Finn, D.P., Dowd, E., Cannabinoids in Parkinson's. Fattore, L., (eds.) Cannabinoids in Neurological and Mental Disease London, 2015, Elsevier Inc., UK.
8. 2 receptor in neurotoxic and inflammation-driven rat models of Parkinson's disease. Exp. Neurol. 269 (2015), 133–141.
9. Deleidi, M., Hallett, P.J., Koprich, J.B., Chung, C.-Y., Isacson, O., The toll-like receptor-3 agonist polyinosinic: polycytidylic acid triggers nigrostriatal dopaminergic degeneration. J. Neurosci. 30 (2010), 16091–16101.
10. Dhillon, A.S., Tarbutton, G.L., Levin, J.L., Plotkin, G.M., Lowry, L.K., Nalbone, J.T., Shepherd, S., Pesticide/environmental exposures and Parkinson's disease in East Texas. J. Agromedicine 13 (2008), 37–48.
11. Ehrhart, J., Obregon, D., Mori, T., Hou, H., Sun, N., Bai, Y., Klein, T., Fernandez, F., Tan, J., Shytle, R., Stimulation of cannabinoid receptor 2 (CB2) suppresses microglial activation. J. Neuroinflammation, 2, 2005, 29.
12. Emmrich, J.V., Hornik, T.C., Neher, J.J., Brown, G.C., Rotenone induces neuronal death by microglial phagocytosis of neurons. FEBS J. 280 (2013), 5030–5038.
13. Esposito, E., Impellizzeri, D., Mazzon, E., Paterniti, I., Cuzzocrea, S., Neuroprotective activities of palmitoylethanolamide in an animal model of Parkinson's disease. PLoS One, 7, 2012, e41880.
14. 125 I] SD7015. Brain Res. Bull. 87 (2012), 504–510.
15. Gao, H.-M., Hong, J.-S., Zhang, W., Liu, B., Distinct role for microglia in rotenone-induced degeneration of dopaminergic neurons. J. Neurosci. 22 (2002), 782–790.
16. Garcia, M.C., Cinquina, V., Palomo-Garo, C., Rabano, A., Fernandez-Ruiz, J., Identification of CB2 receptors in human nigral neurons that degenerate in Parkinson's disease. Neurosci. Lett. 587 (2015), 1–4.
17. Garcia-Ovejero, D., Arevalo-Martin, A., Petrosino, S., Docagne, F., Hagen, C., Bisogno, T., Watanabe, M., Guaza, C., Di Marzo, V., Molina-Holgado, E., The endocannabinoid system is modulated in response to spinal cord injury in rats. Neurobiol. Dis. 33 (2009), 57–71.
18. Gómez-Gálvez, Y., Palomo-Garo, C., Fernández-Ruiz, J., García, C., Potential of the cannabinoid CB 2 receptor as a pharmacological target against inflammation in Parkinson's disease. Prog. Neuro-Psychopharmacol. Biol. Psychiatry, 2015.
19. Gong, J.-P., Onaivi, E.S., Ishiguro, H., Liu, Q.-R., Tagliaferro, P.A., Brusco, A., Uhl, G.R., Cannabinoid CB2 receptors: Immunohistochemical localization in rat brain. Brain Res. 1071 (2006), 10–23.
20. Gonzalez-Aparicio, R., Blanco, E., Serrano, A., Pavon, F.J., Parsons, L.H., Maldonado, R., Robledo, P., Fernandez-Espejo, E., De Fonseca, F.R., The systemic administration of oleoylethanolamide exerts neuroprotection of the nigrostriatal system in experimental parkinsonism. Int. J. Neuropsychopharmacol., 2013, 1–14.
21. Greenamyre, J.T., Betarbet, R., Sherer, T.B., The rotenone model of Parkinson's disease: genes, environment and mitochondria. Parkinsonism Relat. Disord. 9 (2003), 59–64.
22. Hirsch, E.C., Hunot, S., Neuroinflammation in Parkinson's disease: a target for neuroprotection?. Lancet Neurol. 8 (2009), 382–397.
23. Hoban, D.B., Connaughton, E., Connaughton, C., Hogan, G., Thornton, C., Mulcahy, P., Moloney, T.C., Dowd, E., Further characterisation of the LPS model of Parkinson's disease: a comparison of intra-nigral and intra-striatal lipopolysaccharide administration on motor function, microgliosis and nigrostriatal neurodegeneration in the rat. Brain Behav. Immun. 27 (2013), 91–100.
24. Hurley, M., Mash, D., Jenner, P., Expression of cannabinoid CB1 receptor mRNA in basal ganglia of normal and parkinsonian human brain. J. Neural Transm. 110 (2003), 1279–1288.
25. Jang, H., Boltz, D., Sturm-Ramirez, K., Shepherd, K.R., Jiao, Y., Webster, R., Smeyne, R.J., Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration. Proc. Natl. Acad. Sci. 106 (2009), 14063–14068.
26. Jang, H., Boltz, D., Mcclaren, J., Pani, A.K., Smeyne, M., Korff, A., Webster, R., Smeyne, R.J., Inflammatory effects of highly pathogenic H5N1 influenza virus infection in the CNS of mice. J. Neurosci. 32 (2012), 1545–1559.
27. Kerr, D., Burke, N., Ford, G.K., Connor, T., Harhen, B., Egan, L., Finn, D.P., Roche, M., Pharmacological inhibition of endocannabinoid degradation modulates the expression of inflammatory mediators in the hypothalamus following an immunological stressor. Neuroscience 204 (2012), 53–63.
28. Kerr, D., Harhen, B., Okine, B., Egan, L., Finn, D., Roche, M., The monoacylglycerol lipase inhibitor JZL184 attenuates LPS‐induced increases in cytokine expression in the rat frontal cortex and plasma: differential mechanisms of action. Br. J. Pharmacol. 169 (2013), 808–819.
29. Klegeris, A., Bissonnette, C.J., Mcgeer, P.L., Reduction of human monocytic cell neurotoxicity and cytokine secretion by ligands of the cannabinoid‐type CB2 receptor. Br. J. Pharmacol. 139 (2003), 775–786.
30. Lastres‐Becker, I., Cebeira, M., L De Ceballos, M., Zeng, B.Y., Jenner, P., Ramos, J., Fernández‐Ruiz, J., Increased cannabinoid CB1 receptor binding and activation of GTP‐binding proteins in the basal ganglia of patients with Parkinson's syndrome and of MPTP‐treated marmosets. Eur. J. Neurosci. 14 (2001), 1827–1832.
31. Molina-Holgado, F., Pinteaux, E., Heenan, L., Moore, J.D., Rothwell, N.J., Gibson, R.M., Neuroprotective effects of the synthetic cannabinoid HU-210 in primary cortical neurons are mediated by phosphatidylinositol 3-kinase/AKT signaling. Mol. Cell. Neurosci. 28 (2005), 189–194.
32. Mulcahy, P., Walsh, S., Paucard, A., Rea, K., Dowd, E., Characterisation of a novel model of Parkinson's disease by intra-striatal infusion of the pesticide rotenone. Neuroscience 181 (2011), 234–242.
33. Munro, S., Thomas, K.L., Abu-Shaar, M., Molecular Characterization of a Peripheral Receptor for Cannabinoids. 1993.
34. Okine, B., Rea, K., Olango, W., Price, J., Herdman, S., Madasu, M., Roche, M., Finn, D., A role for PPAR‐α in the medial prefrontal cortex in formalin‐evoked nociceptive responding in rats. Br. J. Pharmacol., 2013.
35. Olango, W., Roche, M., Ford, G.K., Harhen, B., Finn, D.P., The endocannabinoid system in the rat dorsolateral periaqueductal grey mediates fear‐conditioned analgesia and controls fear expression in the presence of nociceptive tone. Br. J. Pharmacol. 165 (2012), 2549–2560.
36. Olsson, M., Nikkhah, G., Bentlage, C., Bjorklund, A., Forelimb akinesia in the rat Parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J. Neurosci. 15 (1995), 3863–3875.
37. Onaivi, E.S., Ishiguro, H., Gong, J.P., Patel, S., Perchuk, A., Meozzi, P.A., Myers, L., Mora, Z., Tagliaferro, P., Gardner, E., Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain. Ann. N. Y. Acad. Sci. 1074 (2006), 514–536.
38. Palazuelos, J., Aguado, T., Pazos, M.R., Julien, B., Carrasco, C., Resel, E., Sagredo, O., Benito, C., Romero, J., Azcoitia, I., Microglial CB2 cannabinoid receptors are neuroprotective in Huntington's disease excitotoxicity. Brain 132 (2009), 3152–3164.
39. Panikashvili, D., Simeonidou, C., Ben-Shabat, S., Hanuš, L., Breuer, A., Mechoulam, R., Shohami, E., An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature 413 (2001), 527–531.
40. Périer, C., Marin, C., Jimenez, A., Bonastre, M., Tolosa, E., Hirsch, E.C., Effect of subthalamic nucleus or entopeduncular nucleus lesion on levodopa‐induced neurochemical changes within the basal ganglia and on levodopa‐induced motor alterations in 6‐hydroxydopamine‐lesioned rats. J. Neurochem. 86 (2003), 1328–1337.
41. Pisani, A., Fezza, F., Galati, S., Battista, N., Napolitano, S., Finazzi‐Agrò, A., Bernardi, G., Brusa, L., Pierantozzi, M., Stanzione, P., High endogenous cannabinoid levels in the cerebrospinal fluid of untreated Parkinson's disease patients. Ann. Neurol. 57 (2005), 777–779.
42. Pisani, V., Moschella, V., Bari, M., Fezza, F., Galati, S., Bernardi, G., Stanzione, P., Pisani, A., Maccarrone, M., Dynamic changes of anandamide in the cerebrospinal fluid of Parkinson's disease patients. Mov. Disord. 25 (2010), 920–924.
43. Price, D.A., Martinez, A.A., Seillier, A., Koek, W., Acosta, Y., Fernandez, E., Strong, J.R., Lutz, B., Marsicano, G., Roberts, J.L., WIN55, 212-2, a cannabinoid receptor agonist, protects against nigrostriatal cell loss in the MPTP mouse model of Parkinson's disease. Eur. J. Neurosci., 29, 2009, 2177.
44. Rea, K., Olango, W.M., Okine, B.N., Madasu, M.K., McGuire, I.C., Coyle, K., Harhen, B., Roche, M., Finn, D.P., Impaired endocannabinoid signalling in the rostral ventromedial medulla underpins genotype-dependent hyper-responsivity to noxious stimuli. Pain. 155 (2014), 69–79.
45. Rohn, T.T., Catlin, L.W., Immunolocalization of influenza a virus and markers of inflammation in the human Parkinson's disease brain. PLoS One, 6, 2011, e20495.
46. Schallert, T., Fleming, S.M., Leasure, J.L., Tillerson, J.L., Bland, S.T., CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 39 (2000), 777–787.
47. Scotter, E.L., Abood, M.E., Glass, M., The endocannabinoid system as a target for the treatment of neurodegenerative disease. Br. J. Pharmacol. 160 (2010), 480–498.
48. Sherer, T.B., Betarbet, R., Kim, J.-H., Greenamyre, J.T., Selective microglial activation in the rat rotenone model of Parkinson's disease. Neurosci. Lett. 341 (2003), 87–90.
49. Sherer, T.B., Kim, J.-H., Betarbet, R., Greenamyre, J.T., Subcutaneous rotenone exposure causes highly selective dopaminergic degeneration and α-synuclein aggregation. Exp. Neurol. 179 (2003), 9–16.
50. Shoji, H., Watanabe, M., Itoh, S., Kuwahara, H., Hattori, F., Japanese encephalitis and parkinsonism. J. Neurol. 240 (1993), 59–60.
51. Takahashi, M., Yamada, T., Nakajima, S., Nakajima, K., Yamamoto, T., Okada, H., The substantia nigra is a major target for neurovirulent influenza A virus. J. Exp. Med. 181 (1995), 2161–2169.
52. Tanner, C.M., Kamel, F., Ross, G., Hoppin, J.A., Goldman, S.M., Korell, M., Marras, C., Bhudhikanok, G.S., Kasten, M., Chade, A.R., Rotenone, paraquat, and Parkinson's disease. Environ. Health Perspect. 119 (2011), 866–872.
53. Tansey, M.G., Goldberg, M.S., Neuroinflammation in Parkinson's disease: its role in neuronal death and implications for therapeutic intervention. Neurobiol. Dis. 37 (2010), 510–518.
54. Ternianov, A., Pérez-Ortiz, J.M., Solesio, M.E., García-Gutiérrez, M.S., Ortega-Álvaro, A., Navarrete, F., Leiva, C., Galindo, M.F., Manzanares, J., Overexpression of CB2 cannabinoid receptors results in neuroprotection against behavioral and neurochemical alterations induced by intracaudate administration of 6-hydroxydopamine. Neurobiol. Aging, 33, 2012 (421. e1-421. e16).
55. Van Laere, K., Casteels, C., Lunskens, S., Goffin, K., Grachev, I.D., Bormans, G., Vandenberghe, W., Regional changes in type 1 cannabinoid receptor availability in Parkinson's disease in vivo. Neurobiol. Aging, 33, 2012 (620. e1-620. e8).
56. 1 receptor expression in the 6-hydroxydopamine-induced nigrostriatal terminal lesion model of Parkinson's disease in the rat. Brain Res. Bull. 81 (2010), 543–548.
57. Yiangou, Y., Facer, P., Durrenberger, P., Chessell, I.P., Naylor, A., Bountra, C., Banati, R.R., Anand, P., COX-2, CB2 and P2X7-immunoreactivities are increased in activated microglial cells/macrophages of multiple sclerosis and amyotrophic lateral sclerosis spinal cord. BMC Neurol., 6, 2006, 12.