Cannabinoid receptor CB2 is expressed on vascular cells, but not astroglial cells in the post-mortem human Huntington's disease brain

Journal of Chemical Neuroanatomy

Volumn 59-60, Issue , 2014, Pages 62-71

  Dowie, Megan J ^a,b   Grimsey, Natasha L ^a   Hoffman, Therri ^a   Faull, Richard L M ^a   Glass, Michelle ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Blood brain barrier; Gliosis; Inflammation; Neurodegeneration

Indexed keywords

CALCIUM BINDING PROTEIN; CANNABINOID 2 RECEPTOR; SMOOTH MUSCLE ACTIN; CNR2 PROTEIN, HUMAN;

ARTICLE; ASTROCYTE; CONTROLLED STUDY; DEGENERATIVE DISEASE; HUMAN; HUMAN CELL; HUNTINGTON CHOREA; IMMUNOCOMPETENT CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MICROGLIA; NERVE CELL DEGENERATION; NERVE DEGENERATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; TISSUE PREPARATION; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE; ADULT; AGED; AUTOPSY; BIOSYNTHESIS; CORPUS STRIATUM; ENDOTHELIUM CELL; FEMALE; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY;

ADULT; AGED; ASTROCYTES; AUTOPSY; CORPUS STRIATUM; ENDOTHELIAL CELLS; FEMALE; HUMANS; HUNTINGTON DISEASE; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; RECEPTOR, CANNABINOID, CB2;

EID: 84905994809     PISSN: 08910618     EISSN: 18736300     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2014.06.004     Document Type: Article

References (62)

1. Aguzzi A., Barres B.A., Bennett M.L. Microglia: scapegoat, saboteur, or something else?. Science 2013, 339(6116):156-161.
2. Ashton J.C., Friberg D., Darlington C.L., Smith P.F. Expression of the cannabinoid CB2 receptor in the rat cerebellum: an immunohistochemical study. Neurosci. Lett. 2006, 396(2):113-116.
3. Atwood B.K., Mackie K. CB2: a cannabinoid receptor with an identity crisis. Br. J. Pharmacol. 2010, 160(3):467-479.
4. Ballabh P., Braun A., Nedergaard M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol. Dis. 2004, 16(1):1-13.
5. Bari M., Battista N., Valenza M., Mastrangelo N., Malaponti M., Catanzaro G., Centonze D., Finazzi-Agro A., Cattaneo E., Maccarrone M. In vitro and in vivo models of Huntington's disease show alterations in the endocannabinoid system. FEBS J. 2013, 280(14):3376-3388.
6. Benito C., Nunez E., Tolon R.M., Carrier E.J., Rabano A., Hillard C.J., Romero J. Cannabinoid CB2 receptors and fatty acid amide hydrolase are selectively overexpressed in neuritic plaque-associated glia in Alzheimer's disease brains. J. Neurosci. 2003, 23(35):11136-11141.
7. Benito C., Romero J.P., Tolon 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. 2007, 27(9):2396-2402.
8. Bird E.D., Mackay A.V., Rayner C.N., Iversen L.L. Reduced glutamic-acid-decarboxylase activity of post-mortem brain in Huntington's chorea. Lancet 1973, 1(7812):1090-1092.
9. Blazquez C., Casanova M.L., Planas A., Gomez Del Pulgar T., Villanueva C., Fernandez-Acenero M.J., Aragones J., Huffman J.W., Jorcano J.L., Guzman M. Inhibition of tumor angiogenesis by cannabinoids. FASEB J. 2003, 17(3):529-531.
10. Bouchard J., Truong J., Bouchard K., Dunkelberger D., Desrayaud S., Moussaoui S., Tabrizi S.J., Stella N., Muchowski P.J. Cannabinoid receptor 2 signaling in peripheral immune cells modulates disease onset and severity in mouse models of Huntington's disease. J. Neurosci. 2012, 32(50):18259-18268.
11. Brambilla R., Couch Y., Lambertsen K.L. The effect of stroke on immune function. Mol. Cell. Neurosci. 2013, 53:26-33.
12. Brighton P.J., McDonald J., Taylor A.H., Challiss R.A., Lambert D.G., Konje J.C., Willets J.M. Characterization of anandamide-stimulated cannabinoid receptor signaling in human ULTR myometrial smooth muscle cells. Mol. Endocrinolj 2009, 23(9):1415-1427.
13. Cecyre B., Thomas S., Ptito M., Casanova C., Bouchard J.F. Evaluation of the specificity of antibodies raised against cannabinoid receptor type 2 in the mouse retina. Naunyn Schmiedebergs Arch. Pharmacol. 2013, 387:175-184.
14. Chiba T., Umegaki K. Pivotal roles of monocytes/macrophages in stroke. Mediators Inflamm 2013, 2013:759103.
15. Dowie M.J., Scotter E.L., Molinari E., Glass M. The therapeutic potential of G-protein coupled receptors in Huntington's disease. Pharmacol. Ther. 2010, 128(2):305-323.
16. Ellrichmann G., Reick C., Saft C., Linker R.A. The Role of the Immune System in Huntington's Disease. Clin. Dev. Immunol. 2013, 2013:541259.
17. Fonseca B.M., Correia-da-Silva G., Taylor A.H., Konje J.C., Bell S.C., Teixeira N.A. Spatio-temporal expression patterns of anandamide-binding receptors in rat implantation sites: evidence for a role of the endocannabinoid system during the period of placental development. Reprod. Biol. Endocrinol. 2009, 7:121.
18. Fraga-Silva R.A., Costa-Fraga F.P., Montecucco F., Faye Y., Savergnini S.Q., Lenglet S., Mach F., Steffens S., Stergiopulos N., dos Santos R.A., da Silva R.F. Treatment with CB2 agonist JWH-133 reduces histological features associated with erectile dysfunction in hypercholesterolemic mice. Clin. Dev. Immunol. 2013, 2013:263846.
19. Frank-Cannon T.C., Alto L.T., McAlpine F.E., Tansey M.G. Does neuroinflammation fan the flame in neurodegenerative diseases?. Mol. Neurodegener. 2009, 4:47.
20. Glass M., Dragunow M., Faull R.L. The pattern of neurodegeneration in Huntington's disease: a comparative study of cannabinoid, dopamine, adenosine and GABA(A) receptor alterations in the human basal ganglia in Huntington's disease. Neuroscience 2000, 97(3):505-519.
21. Golech S.A., McCarron R.M., Chen Y., Bembry J., Lenz F., Mechoulam R., Shohami E., Spatz M. Human brain endothelium: coexpression and function of vanilloid and endocannabinoid receptors. Brain Res. Mol. Brain Res. 2004, 132(1):87-92.
22. Graham E.S., Angel C.E., Schwarcz L.E., Dunbar P.R., Glass M. Detailed characterisation of CB2 receptor protein expression in peripheral blood immune cells from healthy human volunteers using flow cytometry. Int. J. Immunopathol. Pharmacol. 2010, 23(1):25-34.
23. Group T.H.s.D.C.R A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 1993, 72(6):971-983.
24. Guillemin G.J., Brew B.J. Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification. J. Leukoc. Biol. 2004, 75(3):388-397.
25. Helliwell R.J., Chamley L.W., Blake-Palmer K., Mitchell M.D., Wu J., Kearn C.S., Glass M. Characterization of the endocannabinoid system in early human pregnancy. J. Clin. Endocrinol. Metab. 2004, 89(10):5168-5174.
26. Li S., Li X.J. Multiple pathways contribute to the pathogenesis of Huntington disease. Mol. Neurodegener. 2006, 1:19.
27. Li C., Zhao R., Gao K., Wei Z., Yin M.Y., Lau L.T., Chui D., Hoi Yu A.C. Astrocytes: implications for neuroinflammatory pathogenesis of Alzheimer's disease. Curr. Alzheimer Res. 2011, 8(1):67-80.
28. Lu T.S., Avraham H.K., Seng S., Tachado S.D., Koziel H., Makriyannis A., Avraham S. Cannabinoids inhibit HIV-1 Gp120-mediated insults in brain microvascular endothelial cells. J. Immunol. 2008, 181(9):6406-6416.
29. Maccarrone M., Battista N., Centonze D. The endocannabinoid pathway in Huntington's disease: a comparison with other neurodegenerative diseases. Prog. Neurobiol. 2007, 81(5-6):349-379.
30. McGeer P.L., McGeer E.G., Fibiger H.C. Glutamic-acid decarboxylase and choline acetylase in Huntington's chorea and Parkinson's disease. Lancet 1973, 2(7829):622-623.
31. Mestre L., Correa F., Docagne F., Clemente D., Guaza C. The synthetic cannabinoid WIN 55,212-2 increases COX-2 expression and PGE2 release in murine brain-derived endothelial cells following Theiler's virus infection. Biochem. Pharmacol. 2006, 72(7):869-880.
32. Minghetti L. Role of inflammation in neurodegenerative diseases. Curr. Opin. Neurol. 2005, 18(3):315-321.
33. Moller T. Neuroinflammation in Huntington's disease. J. Neural Transm. 2010, 117(8):1001-1008.
34. Myers R.H., Vonsattel J.P., Paskevich P.A., Kiely D.K., Stevens T.J., Cupples L.A., Richardson E.P., Bird E.D. Decreased neuronal and increased oligodendroglial densities in Huntington's disease caudate nucleus. J. Neuropathol. Exp. Neurol. 1991, 50(6):729-742.
35. Nunez E., Benito C., Tolon R.M., Hillard C.J., Griffin, Romero J. Glial expression of cannabinoid CB(2) receptors and fatty acid amide hydrolase are beta amyloid-linked events in Down's syndrome. Neuroscience 2008, 151(1):104-110.
36. Pacher P., Hasko G. Endocannabinoids and cannabinoid receptors in ischaemia-reperfusion injury and preconditioning. Br, J. Pharmacol. 2008, 153(2):252-262.
37. Pacher P., Mackie K. Interplay of cannabinoid 2 (CB2) receptors with nitric oxide synthases, oxidative and nitrative stress, and cell death during remote neurodegeneration. J. Mol. Med. 2012, 90(4):347-351.
38. Pacher P., Mechoulam R. Is lipid signaling through cannabinoid 2 receptors part of a protective system?. Prog. Lipid Res. 2011, 50(2):193-211.
39. Palazuelos J., Aguado T., Pazos M.R., Julien B., Carrasco C., Resel E., Sagredo O., Benito C., Romero J., Azcoitia I., Fernandez-Ruiz J., Guzman M., Galve-Roperh I. Microglial CB2 cannabinoid receptors are neuroprotective in Huntington's disease excitotoxicity. Brain 2009, 132(Pt. 11):3152-3164.
40. Parums D.V., Cordell J.L., Micklem K., Heryet A.R., Gatter K.C., Mason D.Y. JC70: a new monoclonal antibody that detects vascular endothelium associated antigen on routinely processed tissue sections. J. Clin. Pathol. 1990, 43(9):752-757.
41. Penney J.B., Young A.B. Quantitative autoradiography of neurotransmitter receptors in Huntington disease. Neurology 1982, 32(12):1391-1395.
42. Perry T.L., Hansen S., Kloster M. Huntington's chorea. Deficiency of gamma-aminobutyric acid in brain. N. Eng. J. Med. 1973, 288(7):337-342.
43. Pusztaszeri M.P., Seelentag W., Bosman F.T. Immunohistochemical expression of endothelial markers CD31, CD34, von Willebrand factor, and Fli-1 in normal human tissues. J. Histochem. Cytochem. 2006, 54(4):385-395.
44. Rajesh M., Mukhopadhyay P., Batkai S., Hasko G., Liaudet L., Huffman J.W., Csiszar A., Ungvari Z., Mackie K., Chatterjee S., Pacher P. CB2-receptor stimulation attenuates TNF-alpha-induced human endothelial cell activation, transendothelial migration of monocytes, and monocyte-endothelial adhesion. Am. J. Physiol. 2007, 293(4):H2210-H2218.
45. Rajesh M., Mukhopadhyay P., Hasko G., Huffman J.W., Mackie K., Pacher P. CB2 cannabinoid receptor agonists attenuate TNF-alpha-induced human vascular smooth muscle cell proliferation and migration. Br. J. Pharmacol. 2008, 153(2):347-357.
46. Ramirez B.G., Blazquez C., Gomez del Pulgar T., Guzman M., de Ceballos M.L. Prevention of Alzheimer's disease pathology by cannabinoids: neuroprotection mediated by blockade of microglial activation. J. Neurosci. 2005, 25(8):1904-1913.
47. Ramirez S.H., Hasko J., Skuba A., Fan S., Dykstra H., McCormick R., Reichenbach N., Krizbai I., Mahadevan A., Zhang M., Tuma R., Son Y.J., Persidsky Y. Activation of cannabinoid receptor 2 attenuates leukocyte-endothelial cell interactions and blood-brain barrier dysfunction under inflammatory conditions. J. Neurosci. 2012, 32(12):4004-4016.
48. Rom S., Zuluaga-Ramirez V., Dykstra H., Reichenbach N.L., Pacher P., Persidsky Y. Selective activation of cannabinoid receptor 2 in leukocytes suppresses their engagement of the brain endothelium and protects the blood-brain barrier. Am. J. Pathol. 2013, 183:1548-1558.
49. Sagredo O., Gonzalez S., Aroyo I., Pazos M.R., Benito C., Lastres-Becker I., Romero J.P., Tolon R.M., Mechoulam R., Brouillet E., Romero J., Fernandez-Ruiz J. Cannabinoid CB2 receptor agonists protect the striatum against malonate toxicity: relevance for Huntington's disease. Glia 2009, 57(11):1154-1167.
50. Sapp E., Kegel K.B., Aronin N., Hashikawa T., Uchiyama Y., Tohyama K., Bhide P.G., Vonsattel J.P., DiFiglia M. Early and progressive accumulation of reactive microglia in the Huntington disease brain. J. Neuropathol. Exp. Neurol. 2001, 60(2):161-172.
51. Schroder B., Elsasser H.P., Schmidt B., Hasilik A. Characterisation of lipofuscin-like lysosomal inclusion bodies from human placenta. FEBS Lett. 2007, 581(1):102-108.
52. Silvestroni A., Faull R.L., Strand A.D., Moller T. Distinct neuroinflammatory profile in post-mortem human Huntington's disease. Neuroreport 2009, 20(12):1098-1103.
53. Simmons D.A., Casale M., Alcon B., Pham N., Narayan N., Lynch G. Ferritin accumulation in dystrophic microglia is an early event in the development of Huntington's disease. Glia 2007, 55(10):1074-1084.
54. Streit W.J., Mrak R.E., Griffin W.S. Microglia and neuroinflammation: a pathological perspective. J. Neuroinflamm. 2004, 1(1):14.
55. Tambuyzer B.R., Ponsaerts P., Nouwen E.J. Microglia: gatekeepers of central nervous system immunology. J. Leukoc. Biol. 2009, 85(3):352-370.
56. Valdeolivas S., Satta V., Pertwee R.G., Fernandez-Ruiz J., Sagredo O. Sativex-like combination of phytocannabinoids is neuroprotective in malonate-lesioned rats, an inflammatory model of Huntington's disease: role of CB1 and CB2 receptors. ACS Chem. Neurosci. 2012, 3(5):400-406.
57. Van Eldik L.J., Thompson W.L., Ralay Ranaivo H., Behanna H.A., Martin Watterson D. Glia proinflammatory cytokine upregulation as a therapeutic target for neurodegenerative diseases: function-based and target-based discovery approaches. Int. Rev. Neurobiol. 2007, 82:277-296.
58. Vonsattel J.P., Myers R.H., Stevens T.J., Ferrante R.J., Bird E.D., Richardson E.P. Neuropathological classification of Huntington's disease. J. Neuropathol. Exp. Neurol. 1985, 44(6):559-577.
59. Waldvogel H.J., Curtis M.A., Baer K., Rees M.I., Faull R.L. Immunohistochemical staining of post-mortem adult human brain sections. Nat. Protoc. 2006, 1(6):2719-2732.
60. Waldvogel H.J., Thu D., Hogg V., Tippett L., Faullt R.L. Selective neurodegeneration, neuropathology and symptom profiles in Huntington's disease. Adv. Exp. Med. Biol. 2012, 769:141-152.
61. Wright S.P. Adjusted P-values for simultaneous inference. Biometrics 1992, 48(4):1005-1013.
62. Zoratti C., Kipmen-Korgun D., Osibow K., Malli R., Graier W.F. Anandamide initiates Ca(2+) signaling via CB2 receptor linked to phospholipase C in calf pulmonary endothelial cells. Br. J. Pharmacol. 2003, 140(8):1351-1362.