Immunoregulation of a CB2 receptor agonist in a murine model of neuroaids

Journal of Neuroimmune Pharmacology

Volumn 5, Issue 3, 2010, Pages 456-468

  Gorantla, Santhi ^a,b   Makarov, Edward ^a   Roy, Deepa ^a   Finke Dwyer, Jennifer ^a   Murrin, L Charles ^a   Gendelman, Howard E ^a   Poluektova, Larisa ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b NEBRASKA MEDICAL CENTER   (United States)

Author keywords

CB2R; HIV 1 associated neurocognitive disorders; human immunodeficiency virus; neuroinflammation

Indexed keywords

CANNABINOID 2 RECEPTOR AGONIST; CHEMOKINE RECEPTOR CCR5; ENDOCANNABINOID; GP1A; HLA DQ ANTIGEN; N (PIPERIDIN 1 YL) 1 (2,4 DICHLOROPHENYL) 1,4 DIHYDRO 6 METHYLINDENO[1,2 C]PYRAZOLE 3 CARBOXAMIDE; UNCLASSIFIED DRUG;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BLOOD BRAIN BARRIER; COGNITION; CONTROLLED STUDY; DRUG MECHANISM; HIV ASSOCIATED DEMENTIA; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOREGULATION; LEUKOCYTE; MACROPHAGE; MOTOR PERFORMANCE; MOUSE; MURINE ACQUIRED IMMUNODEFICIENCY SYNDROME; NERVE CELL NETWORK; NONHUMAN; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; VIRUS ENCEPHALITIS;

AIDS DEMENTIA COMPLEX; ANIMALS; BRAIN; CD4-CD8 RATIO; DISEASE MODELS, ANIMAL; FAS LIGAND PROTEIN; HIV-1; HUMANS; INDENES; MICE; MICE, INBRED BALB C; NEUROIMMUNOMODULATION; PYRAZOLES; RECEPTOR, CANNABINOID, CB2; RECEPTORS, CANNABINOID; RECEPTORS, CCR5; VIRAL LOAD;

EID: 77955981912     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-010-9225-8     Document Type: Article

References (81)

1. BM Ances RJ Ellis 2007 Dementia and neurocognitive disorders due to HIV-1 infection Semin Neurol 27 1 86 92 10.1055/s-2006-956759 17226745
2. A Arevalo-Martin D Garcia-Ovejero O Gomez A Rubio-Araiz B Navarro-Galve C Guaza E Molina-Holgado F Molina-Holgado 2008 CB2 cannabinoid receptors as an emerging target for demyelinating diseases: from neuroimmune interactions to cell replacement strategies Br J Pharmacol 153 2 216 225 10.1038/sj.bjp.0707466 1:CAS:528:DC%2BD1cXovFCkug%3D%3D 17891163
3. JC Ashton M Glass 2007 The cannabinoid CB2 receptor as a target for inflammation-dependent neurodegeneration Curr Neuropharmacol 5 2 73 80 10.2174/157015907780866884 1:CAS:528:DC%2BD2sXmsFemu70%3D 18615177
4. BS Basavarajappa RA Nixon O Arancio 2009 Endocannabinoid system: emerging role from neurodevelopment to neurodegeneration Mini Rev Med Chem 9 4 448 462 10.2174/138955709787847921 1:CAS:528:DC%2BD1MXks1WisLw%3D 19356123
5. C Benito E Nunez RM Tolon EJ Carrier A Rabano CJ Hillard J Romero 2003 Cannabinoid CB2 receptors and fatty acid amide hydrolase are selectively overexpressed in neuritic plaque-associated glia in Alzheimer's disease brains J Neurosci 23 35 11136 11141 1:CAS:528:DC%2BD3sXpvV2gtbw%3D 14657172
6. C Benito WK Kim I Chavarria CJ Hillard K Mackie RM Tolon K Williams J Romero 2005 A glial endogenous cannabinoid system is upregulated in the brains of macaques with simian immunodeficiency virus-induced encephalitis J Neurosci 25 10 2530 2536 10.1523/JNEUROSCI.3923-04.2005 1:CAS:528:DC%2BD2MXis1ygs74%3D 15758162
7. C Benito E Nunez MR Pazos RM Tolon J Romero 2007 The endocannabinoid system and Alzheimer's disease Mol Neurobiol 36 1 75 81 10.1007/s12035-007-8006- 8 1:CAS:528:DC%2BD2sXht12js7fJ 17952652
8. C Benito JP Romero RM Tolon D Clemente F Docagne CJ Hillard C Guaza J Romero 2007 Cannabinoid CB1 and CB2 receptors and fatty acid amide hydrolase are specific markers of plaque cell subtypes in human multiple sclerosis J Neurosci 27 9 2396 2402 10.1523/JNEUROSCI.4814-06.2007 1:CAS:528:DC%2BD2sXjsVymsLY%3D 17329437
9. T Berney RD Molano A Pileggi P Cattan H Li C Ricordi L Inverardi 2001 Patterns of engraftment in different strains of immunodeficient mice reconstituted with human peripheral blood lymphocytes Transplantation 72 1 133 140 10.1097/00007890-200107150-00026 1:STN:280:DC%2BD3MvhvFWluw%3D%3D 11468548
10. F Berrendero A Sanchez A Cabranes C Puerta JA Ramos A Garcia-Merino J Fernandez-Ruiz 2001 Changes in cannabinoid CB(1) receptors in striatal and cortical regions of rats with experimental allergic encephalomyelitis, an animal model of multiple sclerosis Synapse 41 3 195 202 10.1002/syn.1075 1:CAS:528:DC%2BD3MXlslSgtrc%3D 11391780
11. NE Buckley 2008 The peripheral cannabinoid receptor knockout mice: an update Br J Pharmacol 153 2 309 318 10.1038/sj.bjp.0707527 1:CAS:528: DC%2BD1cXovFClug%3D%3D 17965741
12. SH Burstein CA Audette A Breuer WA Devane S Colodner SA Doyle R Mechoulam 1992 Synthetic nonpsychotropic cannabinoids with potent antiinflammatory, analgesic, and leukocyte antiadhesion activities J Med Chem 35 17 3135 3141 10.1021/jm00095a007 1:CAS:528:DyaK38XltlWgurc%3D 1507202
13. GA Cabral L Griffin-Thomas 2008 Cannabinoids as therapeutic agents for ablating neuroinflammatory disease Endocr Metab Immune Disord Drug Targets 8 3 159 172 10.2174/187153008785700118 1:CAS:528:DC%2BD1cXpvVOgurc%3D 18782012
14. GA Cabral KN Harmon SJ Carlisle 2001 Cannabinoid-mediated inhibition of inducible nitric oxide production by rat microglial cells: evidence for CB1 receptor participation Adv Exp Med Biol 493 207 214 10.1007/0-306-47611-8-24 1:CAS:528:DC%2BD38Xmtlyku7o%3D 11727767
15. GA Cabral ES Raborn L Griffin J Dennis F Marciano-Cabral 2008 CB2 receptors in the brain: role in central immune function Br J Pharmacol 153 2 240 251 10.1038/sj.bjp.0707584 1:CAS:528:DC%2BD1cXovFCltw%3D%3D 18037916
16. D Centonze S Rossi A Finazzi-Agro G Bernardi M Maccarrone 2007 The (endo)cannabinoid system in multiple sclerosis and amyotrophic lateral sclerosis Int Rev Neurobiol 82 171 186 10.1016/S0074-7742(07)82009-5 1:CAS:528: DC%2BD2sXhtVWqs77O 17678961
17. F Correa F Docagne L Mestre F Loria M Hernangomez J Borrell C Guaza 2007 Cannabinoid system and neuroinflammation: implications for multiple sclerosis Neuroimmunomodulation 14 3-4 182 187 10.1159/000110644 1:CAS:528: DC%2BD2sXhsVagsLjI 18073512
18. M Cota M Mengozzi E Vicenzi P Panina-Bordignon F Sinigaglia P Transidico S Sozzani A Mantovani G Poli 2000 Selective inhibition of HIV replication in primary macrophages but not T lymphocytes by macrophage-derived chemokine Proc Natl Acad Sci U S A 97 16 9162 9167 10.1073/pnas.160359197 1:CAS:528: DC%2BD3cXls12ksL4%3D 10908681
19. J Dhein H Walczak C Baumler KM Debatin PH Krammer 1995 Autocrine T-cell suicide mediated by APO-1/(Fas/CD95) Nature 373 6513 438 441 10.1038/373438a0 1:CAS:528:DyaK2MXjsFCjsL4%3D 7530335
20. F Docagne L Mestre F Loria M Hernangomez F Correa C Guaza 2008 Therapeutic potential of CB2 targeting in multiple sclerosis Expert Opin Ther Targets 12 2 185 195 10.1517/14728222.12.2.185 1:CAS:528:DC%2BD1cXovFCqsA%3D%3D 18208367
21. D Eggert PK Dash N Serradji CZ Dong P Clayette F Heymans H Dou S Gorantla HA Gelbard L Poluektova, et al. 2009 Development of a platelet-activating factor antagonist for HIV-1 associated neurocognitive disorders J Neuroimmunol 213 1-2 47 59 10.1016/j.jneuroim.2009.06.002 1:CAS:528:DC%2BD1MXps1Whs7Y%3D 19541372
22. D Eggert PK Dash S Gorantla H Dou G Schifitto SB Maggirwar S Dewhurst L Poluektova HA Gelbard HE Gendelman 2010 Neuroprotective activities of CEP-1347 in models of neuroAIDS J Immunol 184 2 746 756 10.4049/jimmunol.0902962 1:CAS:528:DC%2BC3cXhslCmtw%3D%3D 19966207
23. J Ehrhart D Obregon T Mori H Hou N Sun Y Bai T Klein F Fernandez J Tan RD Shytle 2005 Stimulation of cannabinoid receptor 2 (CB2) suppresses microglial activation J Neuroinflammation 2 29 10.1186/1742-2094-2-29 16343349
24. F Facchinetti E Del Giudice S Furegato M Passarotto A Leon 2003 Cannabinoids ablate release of TNFalpha in rat microglial cells stimulated with lipopolysaccharide Glia 41 2 161 168 10.1002/glia.10177 12509806
25. S Galiegue S Mary J Marchand D Dussossoy D Carriere P Carayon M Bouaboula D Shire G Le Fur P Casellas 1995 Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations Eur J Biochem 232 1 54 61 10.1111/j.1432-1033.1995.tb20780.x 1:CAS:528: DyaK2MXnvVKksL8%3D 7556170
26. HE Gendelman Y Persidsky A Ghorpade J Limoges M Stins M Fiala R Morrisett 1997 The neuropathogenesis of the AIDS dementia complex Aids 11 Suppl A 35 45
27. Gendelman HE, Diesing S, Gelbard H, Swindells S (2004) The neuropathogenesis of HIV-1 infection. Elsevier, London, pp 95-116
28. JP Goldman MP Blundell L Lopes C Kinnon JP Di Santo AJ Thrasher 1998 Enhanced human cell engraftment in mice deficient in RAG2 and the common cytokine receptor gamma chain Br J Haematol 103 2 335 342 10.1046/j.1365-2141. 1998.00980.x 1:CAS:528:DyaK1cXnvFOisL4%3D 9827902
29. W Gonsiorek D Hesk SC Chen D Kinsley JS Fine JV Jackson LA Bober G Deno H Bian J Fossetta, et al. 2006 Characterization of peripheral human cannabinoid receptor (hCB2) expression and pharmacology using a novel radioligand, [35S]Sch225336 J Biol Chem 281 38 28143 28151 10.1074/jbc.M602364200 1:CAS:528:DC%2BD28XpsFOru74%3D 16754676
30. S Gorantla J Liu H Sneller H Dou A Holguin L Smith T Ikezu DJ Volsky L Poluektova HE Gendelman 2007 Copolymer-1 induces adaptive immune anti-inflammatory glial and neuroprotective responses in a murine model of HIV-1 encephalitis J Immunol 179 7 4345 4356 1:CAS:528:DC%2BD2sXhtVCrtbvP 17878329
31. NC Gorin S Piantadosi M Stull H Bonte JR Wingard C Civin 2002 Increased risk of lethal graft-versus-host disease-like syndrome after transplantation into NOD/SCID mice of human mobilized peripheral blood stem cells, as compared to bone marrow or cord blood J Hematother Stem Cell Res 11 2 277 292 10.1089/152581602753658466 11983099
32. DR Green N Droin M Pinkoski 2003 Activation-induced cell death in T cells Immunol Rev 193 70 81 10.1034/j.1600-065X.2003.00051.x 1:CAS:528: DC%2BD3sXkslemsLw%3D 12752672
33. G Hoffmann-Fezer C Gall U Zengerle B Kranz S Thierfelder 1993 Immunohistology and immunocytology of human T-cell chimerism and graft-versus-host disease in SCID mice Blood 81 12 3440 3448 1:STN:280:DyaK3s3otlKqug%3D%3D 8099506
34. W Huppes H Fickenscher BA tHart B Fleckenstein 1994 Cytokine dependence of human to mouse graft-versus-host disease Scand J Immunol 40 1 26 36 10.1111/j.1365-3083.1994.tb03429.x 1:CAS:528:DyaK2cXlsFGltb4%3D 7913246
35. ST Ju DJ Panka H Cui R Ettinger M el-Khatib DH Sherr BZ Stanger A Marshak-Rothstein 1995 Fas(CD95)/FasL interactions required for programmed cell death after T-cell activation Nature 373 6513 444 448 10.1038/373444a0 1:CAS:528:DyaK2MXjsFCjsLw%3D 7530337
36. M Kaul SA Lipton 2006 Mechanisms of neuronal injury and death in HIV-1 associated dementia Curr HIV Res 4 3 307 318 10.2174/157016206777709384 1:CAS:528:DC%2BD28XmvV2mtrk%3D 16842083
37. M Kaul J Zheng S Okamoto HE Gendelman SA Lipton 2005 HIV-1 infection and AIDS: consequences for the central nervous system Cell Death Differ 12 Suppl 1 878 892 10.1038/sj.cdd.4401623 1:CAS:528:DC%2BD2MXlsFOmt7Y%3D 15832177
38. TW Klein CA Newton 2007 Therapeutic potential of cannabinoid-based drugs Adv Exp Med Biol 601 395 413 17713029
39. FR Kreitzer N Stella 2009 The therapeutic potential of novel cannabinoid receptors Pharmacol Ther 122 2 83 96 10.1016/j.pharmthera.2009.01.005 1:CAS:528:DC%2BD1MXkslyktro%3D 19248809
40. I Lastres-Becker F Molina-Holgado JA Ramos R Mechoulam J Fernandez-Ruiz 2005 Cannabinoids provide neuroprotection against 6-hydroxydopamine toxicity in vivo and in vitro: relevance to Parkinson's disease Neurobiol Dis 19 1-2 96 107 10.1016/j.nbd.2004.11.009 1:CAS:528:DC%2BD2MXjtlajsrc%3D 15837565
41. M Leonelli AS Torrao LR Britto 2009 Unconventional neurotransmitters, neurodegeneration and neuroprotection Braz J Med Biol Res 42 1 68 75 10.1590/S0100-879X2009000100011 1:CAS:528:DC%2BD1MXjvV2jsLY%3D 19219299
42. P Loetscher M Uguccioni L Bordoli M Baggiolini B Moser C Chizzolini JM Dayer 1998 CCR5 is characteristic of Th1 lymphocytes Nature 391 6665 344 345 10.1038/34814 1:CAS:528:DyaK1cXot1GlsA%3D%3D 9450746
43. C Lombard M Nagarkatti P Nagarkatti 2007 CB2 cannabinoid receptor agonist, JWH-015, triggers apoptosis in immune cells: potential role for CB2-selective ligands as immunosuppressive agents Clin Immunol 122 3 259 270 10.1016/j.clim.2006.11.002 1:CAS:528:DC%2BD2sXhs1Chu7k%3D 17185040
44. CA Lunn EP Reich L Bober 2006 Targeting the CB2 receptor for immune modulation Expert Opin Ther Targets 10 5 653 663 10.1517/14728222.10.5.653 1:CAS:528:DC%2BD28Xps1ahs7Y%3D 16981823
45. CA Lunn EP Reich JS Fine B Lavey JA Kozlowski RW Hipkin DJ Lundell L Bober 2008 Biology and therapeutic potential of cannabinoid CB2 receptor inverse agonists Br J Pharmacol 153 2 226 239 10.1038/sj.bjp.0707480 1:CAS:528:DC%2BD1cXovFCktw%3D%3D 17906679
46. K Mackie N Stella 2006 Cannabinoid receptors and endocannabinoids: evidence for new players AAPS J 8 2 E298 E306 16796380
47. MCG Marcondes EME Burudi S Huitron-Resendiz M Sanchez-Alavez D Watry M Zandonatti SJ Henriksen HS Fox 2001 Highly activated CD8+ T cells in the brain correlate with early central nervous system dysfunction in simian immunodeficiency virus infection J Immunol 167 9 5429 5438 1:CAS:528: DC%2BD3MXotVWjt7s%3D 11673562
48. MC Marcondes CA Phillipson HS Fox 2003 Distinct clonal repertoire of brain CD8+ cells in simian immunodeficiency virus infection AIDS 17 11 1605 1611 10.1097/00002030-200307250-00004 1:CAS:528:DC%2BD3sXlsVynu7o%3D 12853742
49. L Mestre F Docagne F Correa F Loria M Hernangomez J Borrell C Guaza 2009 A cannabinoid agonist interferes with the progression of a chronic model of multiple sclerosis by downregulating adhesion molecules Mol Cell Neurosci 40 2 258 266 10.1016/j.mcn.2008.10.015 1:CAS:528:DC%2BD1MXhs1aku70%3D 19059482
50. G Murineddu P Lazzari S Ruiu A Sanna G Loriga I Manca M Falzoi C Dessi MM Curzu G Chelucci, et al. 2006 Tricyclic pyrazoles. 4. Synthesis and biological evaluation of analogues of the robust and selective CB2 cannabinoid ligand 1-(2′, 4′-dichlorophenyl)-6-methyl-N-piperidin-1-yl-1, 4-dihydroindeno[1, 2-c ]pyrazole-3-carboxamide J Med Chem 49 25 7502 7512 10.1021/jm060920d 1:CAS:528:DC%2BD28Xht1WhsL%2FJ 17149879
51. ES Onaivi 2009 Cannabinoid receptors in brain: pharmacogenetics, neuropharmacology, neurotoxicology, and potential therapeutic applications Int Rev Neurobiol 88 335 369 10.1016/S0074-7742(09)88012-4 1:CAS:528: DC%2BC3cXmt1Omsg%3D%3D 19897083
52. MA Ostrowski SJ Justement A Catanzaro CA Hallahan LA Ehler SB Mizell PN Kumar JA Mican TW Chun AS Fauci 1998 Expression of chemokine receptors CXCR4 and CCR5 in HIV-1-infected and uninfected individuals J Immunol 161 6 3195 3201 1:CAS:528:DyaK1cXmtVGlsb0%3D 9743388
53. P Pacher S Batkai G Kunos 2006 The endocannabinoid system as an emerging target of pharmacotherapy Pharmacol Rev 58 3 389 462 10.1124/pr.58.3.2 1:CAS:528:DC%2BD28XhtVOhtLfO 16968947
54. KD Patel JS Davison QJ Pittman KA Sharkey 2010 Cannabinoid CB(2) receptors in health and disease Curr Med Chem 17 14 1394 1410 10.2174/092986710790980041 1:CAS:528:DC%2BC3cXmtFehtLk%3D
55. T Pearson DL Greiner LD Shultz 2008 Humanized SCID mouse models for biomedical research Curr Top Microbiol Immunol 324 25 51 10.1007/978-3-540- 75647-7-2 1:CAS:528:DC%2BD1cXosFGnsrw%3D 18481451
56. S Pino MA Brehm L Covassin-Barberis M King B Gott TH Chase J Wagner L Burzenski O Foreman DL Greiner, et al. 2010 Development of novel major histocompatibility complex class I and class II-deficient NOD-SCID IL2R gamma chain knockout mice for modeling human xenogeneic graft-versus-host disease Methods Mol Biol 602 105 117 10.1007/978-1-60761-058-8-7 1:CAS:528: DC%2BC3cXoslyqsb8%3D 20012395
57. D Piomelli 2005 The endocannabinoid system: a drug discovery perspective Curr Opin Investig Drugs 6 7 672 679 1:CAS:528:DC%2BD2MXms1ejsL8%3D 16044662
58. LY Poluektova DH Munn Y Persidsky HE Gendelman 2002 Generation of cytotoxic T cells against virus-infected human brain macrophages in a murine model of HIV-1 encephalitis J Immunol 168 8 3941 3949 1:CAS:528: DC%2BD38XivV2isrY%3D 11937550
59. L Poluektova S Gorantla J Faraci K Birusingh H Dou HE Gendelman 2004 Neuroregulatory events follow adaptive immune-mediated elimination of HIV-1-infected macrophages: studies in a murine model of viral encephalitis J Immunol 172 12 7610 7617 1:CAS:528:DC%2BD2cXks1agsro%3D 15187141
60. Poluektova LY, Gorantla S, Gendelman HE (2004b) Studies of adaptive immunity in a murine model of HIV-1 encephalitis. In: Gendelman HE, Grant I, Lipton S, Swindells S (eds) Neurology of AIDS. Oxford University Press, Oxford
61. R Potula L Poluektova B Knipe J Chrastil D Heilman H Dou O Takikawa DH Munn HE Gendelman Y Persidsky 2005 Inhibition of indoleamine 2, 3-dioxygenase (IDO) enhances elimination of virus-infected macrophages in an animal model of HIV-1 encephalitis Blood 106 7 2382 2390 10.1182/blood-2005-04-1403 1:CAS:528:DC%2BD2MXhtVKqt7zJ 15961516
62. DA Price AA Martinez A Seillier W Koek Y Acosta E Fernandez R Strong B Lutz G Marsicano JL Roberts, et al. 2009 WIN55, 212-2, a cannabinoid receptor agonist, protects against nigrostriatal cell loss in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine mouse model of Parkinson's disease Eur J Neurosci 29 11 2177 2186 10.1111/j.1460-9568.2009.06764.x 19490092
63. RA Puffenbarger AC Boothe GA Cabral 2000 Cannabinoids inhibit LPS-inducible cytokine mRNA expression in rat microglial cells Glia 29 1 58 69 10.1002/(SICI)1098-1136(20000101)29:1<58::AID-GLIA6>3.0.CO;2-W 1:STN:280:DC%2BD3c%2Fmt1Orsg%3D%3D 10594923
64. S Qin JB Rottman P Myers N Kassam M Weinblatt M Loetscher AE Koch B Moser CR Mackay 1998 The chemokine receptors CXCR3 and CCR5 mark subsets of T cells associated with certain inflammatory reactions J Clin Invest 101 4 746 754 10.1172/JCI1422 1:CAS:528:DyaK1cXht1Wrsbk%3D 9466968
65. RB Rock G Gekker S Hu WS Sheng GA Cabral BR Martin PK Peterson 2007 WIN55, 212-2-mediated inhibition of HIV-1 expression in microglial cells: involvement of cannabinoid receptors J Neuroimmune Pharmacol 2 2 178 183 10.1007/s11481-006-9040-4 18040842
66. K Rostasy L Monti C Yiannoutsos M Kneissl J Bell TL Kemper JC Hedreen BA Navia 1999 Human immunodeficiency virus infection, inducible nitric oxide synthase expression, and microglial activation: pathogenetic relationship to the acquired immunodeficiency syndrome dementia complex Ann Neurol 46 2 207 216 10.1002/1531-8249(199908)46:2<207::AID-ANA10>3.0.CO;2-4 1:STN:280:DyaK1MzntFCrtA%3D%3D 10443886
67. S Roychowdhury BW Blaser AG Freud K Katz D Bhatt AK Ferketich V Bergdall D Kusewitt RA Baiocchi MA Caligiuri 2005 IL-15 but not IL-2 rapidly induces lethal xenogeneic graft-versus-host disease Blood 106 7 2433 2435 10.1182/blood-2005-04-1597 1:CAS:528:DC%2BD2MXhtVKqt73N 15976176
68. E Ryberg N Larsson S Sjogren S Hjorth NO Hermansson J Leonova T Elebring K Nilsson T Drmota PJ Greasley 2007 The orphan receptor GPR55 is a novel cannabinoid receptor Br J Pharmacol 152 7 1092 1101 10.1038/sj.bjp.0707460 1:CAS:528:DC%2BD2sXhtlCrsbnI 17876302
69. MK Schneider KO Gronvik 1995 Acute graft-versus-host reaction in SCID mice leads to an abnormal expansion of CD8+ V beta 14+ and a broad inactivation of donor T cells followed by a host-restricted tolerance and a normalization of the TCR V beta repertoire in the chronic phase Scand J Immunol 41 4 373 383 10.1111/j.1365-3083.1995.tb03581.x 1:CAS:528:DyaK2MXlsVeqs7g%3D 7899825
70. JL Shoemaker KA Seely RL Reed JP Crow PL Prather 2007 The CB2 cannabinoid agonist AM-1241 prolongs survival in a transgenic mouse model of amyotrophic lateral sclerosis when initiated at symptom onset J Neurochem 101 1 87 98 10.1111/j.1471-4159.2006.04346.x 1:CAS:528:DC%2BD2sXksFSqsb4%3D 17241118
71. DG Smith GJ Guillemin L Pemberton S Kerr A Nath GA Smythe BJ Brew 2001 Quinolinic acid is produced by macrophages stimulated by platelet activating factor, Nef and Tat J NeuroVirol 7 1 56 60 10.1080/135502801300069692 1:CAS:528:DC%2BD3MXnt1Orurk%3D 11519483
72. S Steffens NR Veillard C Arnaud G Pelli F Burger C Staub M Karsak A Zimmer JL Frossard F Mach 2005 Low dose oral cannabinoid therapy reduces progression of atherosclerosis in mice Nature 434 7034 782 786 10.1038/nature03389 1:CAS:528:DC%2BD2MXivFCgtbs%3D 15815632
73. N Stella 2009 Endocannabinoid signaling in microglial cells Neuropharmacology 56 Suppl 1 244 253 10.1016/j.neuropharm.2008.07.037 1:CAS:528:DC%2BD1MXhsVKhsg%3D%3D 18722389
74. T Takahashi M Tanaka CI Brannan NA Jenkins NG Copeland T Suda S Nagata 1994 Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand Cell 76 6 969 976 10.1016/0092-8674(94)90375-1 1:CAS:528:DyaK2cXksFGlu7g%3D 7511063
75. M Tary-Lehmann PV Lehmann D Schols MG Roncarolo A Saxon 1994 Anti-SCID mouse reactivity shapes the human CD4+ T cell repertoire in hu-PBL-SCID chimeras J Exp Med 180 5 1817 1827 10.1084/jem.180.5.1817 1:STN:280: DyaK2M%2FltlOisA%3D%3D 7964463
76. GA Thakur R Tichkule S Bajaj A Makriyannis 2009 Latest advances in cannabinoid receptor agonists Expert Opin Ther Pat 19 12 1647 1673 10.1517/13543770903436505 1:CAS:528:DC%2BD1MXhs1WhtLfP 19939187
77. KG Tournoy S Depraetere RA Pauwels GG Leroux-Roels 2000 Mouse strain and conditioning regimen determine survival and function of human leucocytes in immunodeficient mice Clin Exp Immunol 119 1 231 239 10.1046/j.1365-2249.2000. 01099.x 1:STN:280:DC%2BD3c%2FnsVymtQ%3D%3D 10606988
78. R Van Duyne C Pedati I Guendel L Carpio K Kehn-Hall M Saifuddin F Kashanchi 2009 The utilization of humanized mouse models for the study of human retroviral infections Retrovirology 6 1 76 10.1186/1742-4690-6-76 19674458
79. SF Verlinden AH Mulder JP de Leeuw DW van Bekkum 1998 T lymphocytes determine the development of xeno GVHD and of human hemopoiesis in NOD/SCID mice following human umbilical cord blood transplantation Stem Cells 16 Suppl 1 205 217 11012164
80. Y Waksman JM Olson SJ Carlisle GA Cabral 1999 The central cannabinoid receptor (CB1) mediates inhibition of nitric oxide production by rat microglial cells J Pharmacol Exp Ther 288 3 1357 1366 1:CAS:528:DyaK1MXhs1KisLg%3D 10027878
81. H Xu CL Cheng M Chen A Manivannan L Cabay RG Pertwee A Coutts JV Forrester 2007 Anti-inflammatory property of the cannabinoid receptor-2-selective agonist JWH-133 in a rodent model of autoimmune uveoretinitis J Leukoc Biol 82 3 532 541 10.1189/jlb.0307159 1:CAS:528:DC%2BD2sXhtValu7rM 17537989