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The CB2 receptor and its role as a regulator of inflammation

The CB2 receptor and its role as a regulator of inflammation The CB2 receptor is the peripheral receptor for cannabinoids. It is mainly expressed in immune tissues, highlighting the possibility that the endocannabinoid system has an immunomodulatory role. In this respect, the CB2 receptor was shown to modulate immune cell functions, both in cellulo and in animal models of inflammatory diseases. In this regard, numerous studies have reported that mice lacking the CB2 receptor have an exacerbated inflammatory phenotype. This suggests that therapeutic strategies aiming at modulating CB2 signaling could be promising for the treatment of various inflammatory conditions. Herein, we review the pharmacology of the CB2 receptor, its expression pattern, and the signaling pathways induced by its activation. We next examine the regulation of immune cell functions by the CB2 receptor and the evidence obtained from primary human cells, immortalized cell lines, and animal models of inflammation. Finally, we discuss the possible therapies targeting the CB2 receptor and the questions that remain to be addressed to determine whether this receptor could be a potential target to treat inflammatory disease. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Cellular and Molecular Life Sciences Springer Journals

The CB2 receptor and its role as a regulator of inflammation

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Publisher
Springer Journals
Copyright
Copyright © 2016 by The Author(s)
Subject
Life Sciences; Cell Biology; Biomedicine, general; Life Sciences, general; Biochemistry, general
ISSN
1420-682X
eISSN
1420-9071
DOI
10.1007/s00018-016-2300-4
pmid
27402121
Publisher site
See Article on Publisher Site

Abstract

The CB2 receptor is the peripheral receptor for cannabinoids. It is mainly expressed in immune tissues, highlighting the possibility that the endocannabinoid system has an immunomodulatory role. In this respect, the CB2 receptor was shown to modulate immune cell functions, both in cellulo and in animal models of inflammatory diseases. In this regard, numerous studies have reported that mice lacking the CB2 receptor have an exacerbated inflammatory phenotype. This suggests that therapeutic strategies aiming at modulating CB2 signaling could be promising for the treatment of various inflammatory conditions. Herein, we review the pharmacology of the CB2 receptor, its expression pattern, and the signaling pathways induced by its activation. We next examine the regulation of immune cell functions by the CB2 receptor and the evidence obtained from primary human cells, immortalized cell lines, and animal models of inflammation. Finally, we discuss the possible therapies targeting the CB2 receptor and the questions that remain to be addressed to determine whether this receptor could be a potential target to treat inflammatory disease.

Journal

Cellular and Molecular Life Sciences – Springer Journals

Published: Jul 11, 2016

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  • 2-Arachidonoylglycerol, an endogenous cannabinoid receptor ligand, enhances the adhesion of HL-60 cells differentiated into macrophage-like cells and human peripheral blood monocytes
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  • Effect of lipid rafts on CB2 receptor signaling and 2-arachidonoyl-glycerol metabolism in human immune cells
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  • Cannabinoid receptors can activate and inhibit G protein-coupled inwardly rectifying potassium channels in a xenopus oocyte expression system
    McAllister, SD; Griffin, G; Satin, LS; Abood, ME
  • CB2 cannabinoid receptor targets mitogenic Gi protein-cyclin D1 axis in osteoblasts
    Ofek, O; Attar-Namdar, M; Kram, V; Dvir-Ginzberg, M; Mechoulam, R; Zimmer, A; Frenkel, B; Shohami, E; Bab, I
  • Celastrol-induced apoptosis in human HaCaT keratinocytes involves the inhibition of NF-kappaB activity
    Zhou, LL; Lin, ZX; Fung, KP; Cheng, CH; Che, CT; Zhao, M; Wu, SH; Zuo, Z
  • Activation of cannabinoid receptor 2 reduces inflammation in acute experimental pancreatitis via intra-acinar activation of p38 and MK2-dependent mechanisms
    Michler, T; Storr, M; Kramer, J; Ochs, S; Malo, A; Reu, S; Goke, B; Schafer, C
  • Anandamide initiates Ca2+ signaling via CB2 receptor linked to phospholipase C in calf pulmonary endothelial cells
    Zoratti, C; Kipmen-Korgun, D; Osibow, K; Malli, R; Graier, WF
  • Characterization of human cannabinoid CB2 receptor coupled to chimeric Galpha(qi5) and Galpha(qo5) proteins
    Malysz, J; Daza, AV; Kage, K; Grayson, GK; Yao, BB; Meyer, MD; Gopalakrishnan, M
  • Regulation of inflammation by cannabinoids, the endocannabinoids 2-arachidonoyl-glycerol and arachidonoyl-ethanolamide, and their metabolites
    Turcotte, C; Chouinard, F; Lefebvre, JS; Flamand, N
  • Effect of anandamide uptake inhibition in the production of nitric oxide and in the release of cytokines in astrocyte cultures
    Ortega-Gutierrez, S; Molina-Holgado, E; Guaza, C
  • Distinct modulation of human myeloid and plasmacytoid dendritic cells by anandamide in multiple sclerosis
    Chiurchiu, V; Cencioni, MT; Bisicchia, E; Bardi, M; Gasperini, C; Borsellino, G; Centonze, D; Battistini, L; Maccarrone, M
  • The endocannabinoid anandamide protects neurons during CNS inflammation by induction of MKP-1 in microglial cells
    Eljaschewitsch, E; Witting, A; Mawrin, C; Lee, T; Schmidt, PM; Wolf, S; Hoertnagl, H; Raine, CS; Schneider-Stock, R; Nitsch, R; Ullrich, O
  • Anandamide enhances IL-10 production in activated microglia by targeting CB2 receptors: roles of ERK1/2, JNK, and NF-kappaB
    Correa, F; Hernangomez, M; Mestre, L; Loria, F; Spagnolo, A; Docagne, F; Marzo, V; Guaza, C
  • The endocannabinoid anandamide downregulates IL-23 and IL-12 subunits in a viral model of multiple sclerosis: evidence for a cross-talk between IL-12p70/IL-23 axis and IL-10 in microglial cells
    Correa, F; Hernangomez-Herrero, M; Mestre, L; Loria, F; Docagne, F; Guaza, C
  • Anandamide, acting via CB2 Receptors, alleviates LPS-induced neuroinflammation in rat primary microglial cultures
    Malek, N; Popiolek-Barczyk, K; Mika, J; Przewlocka, B; Starowicz, K
  • Anandamide and Δ9-tetrahydrocannabinol directly inhibit cells of the immune system via CB2 receptors
    Eisenstein, TK; Meissler, JJ; Wilson, Q; Gaughan, JP; Adler, MW
  • Anandamide suppresses proliferation and cytokine release from primary human T-lymphocytes mainly via CB2 receptors
    Cencioni, MT; Chiurchiu, V; Catanzaro, G; Borsellino, G; Bernardi, G; Battistini, L; Maccarrone, M
  • Temporal variation in CB2R levels following T lymphocyte activation: evidence that cannabinoids modulate CXCL12-induced chemotaxis
    Coopman, K; Smith, LD; Wright, KL; Ward, SG
  • Anandamide is an endogenous inhibitor for the migration of tumor cells and T lymphocytes
    Joseph, J; Niggemann, B; Zaenker, KS; Entschladen, F
  • Distinct expression profiles of the peripheral cannabinoid receptor in lymphoid tissues depending on receptor activation status
    Rayman, N; Lam, KH; Laman, JD; Simons, PJ; Lowenberg, B; Sonneveld, P; Delwel, R
  • Hematopoietic cells expressing the peripheral cannabinoid receptor migrate in response to the endocannabinoid 2-arachidonoylglycerol
    Jorda, MA; Verbakel, SE; Valk, PJ; Vankan-Berkhoudt, YV; Maccarrone, M; Finazzi-Agro, A; Lowenberg, B; Delwel, R
  • Induction of preferential chemotaxis of unstimulated B-lymphocytes by 2-arachidonoylglycerol in immunized mice
    Tanikawa, T; Kurohane, K; Imai, Y
  • The endogenous cannabinoid 2-arachidonoyl glycerol as in vivo chemoattractant for dendritic cells and adjuvant for Th1 response to a soluble protein
    Maestroni, GJ
  • Chemotaxis of human peripheral blood eosinophils to 2-arachidonoylglycerol: comparison with other eosinophil chemoattractants
    Kishimoto, S; Oka, S; Gokoh, M; Sugiura, T
  • Involvement of cannabinoid receptor CB2 in dectin-1-mediated macrophage phagocytosis
    Shiratsuchi, A; Watanabe, I; Yoshida, H; Nakanishi, Y
  • 2-arachidonoylglycerol induces the migration of HL-60 cells differentiated into macrophage-like cells and human peripheral blood monocytes through the cannabinoid CB2 receptor-dependent mechanism
    Kishimoto, S; Gokoh, M; Oka, S; Muramatsu, M; Kajiwara, T; Waku, K; Sugiura, T
  • 2-Arachidonoylglycerol, an endogenous cannabinoid receptor ligand, induces accelerated production of chemokines in HL-60 cells
    Kishimoto, S; Kobayashi, Y; Oka, S; Gokoh, M; Waku, K; Sugiura, T
  • Nonpsychotropic cannabinoid receptors regulate microglial cell migration
    Walter, L; Franklin, A; Witting, A; Wade, C; Xie, Y; Kunos, G; Mackie, K; Stella, N
  • 2-Arachidonoylglycerol, an endogenous cannabinoid receptor ligand, induces rapid actin polymerization in HL-60 cells differentiated into macrophage-like cells
    Gokoh, M; Kishimoto, S; Oka, S; Mori, M; Waku, K; Ishima, Y; Sugiura, T
  • Endogenous cannabinoid receptor ligand induces the migration of human natural killer cells
    Kishimoto, S; Muramatsu, M; Gokoh, M; Oka, S; Waku, K; Sugiura, T
  • 2-Arachidonoylglycerol modulates human endothelial cell/leukocyte interactions by controlling selectin expression through CB1 and CB2 receptors
    Gasperi, V; Evangelista, D; Chiurchiu, V; Florenzano, F; Savini, I; Oddi, S; Avigliano, L; Catani, MV; Maccarrone, M
  • WIN55,212-2-mediated inhibition of HIV-1 expression in microglial cells: involvement of cannabinoid receptors
    Rock, RB; Gekker, G; Hu, S; Sheng, WS; Cabral, GA; Martin, BR; Peterson, PK
  • Synthetic cannabinoid WIN55,212-2 inhibits generation of inflammatory mediators by IL-1β-stimulated human astrocytes
    Sheng, WS; Hu, S; Min, X; Cabral, GA; Lokensgard, JR; Peterson, PK
  • Activation through cannabinoid receptors 1 and 2 on dendritic cells triggers NF-κB-dependent apoptosis: novel role for endogenous and exogenous cannabinoids in immunoregulation
    Do, Y; McKallip, RJ; Nagarkatti, M; Nagarkatti, PS
  • Signaling through cannabinoid receptor 2 suppresses murine dendritic cell migration by inhibiting matrix metalloproteinase 9 expression
    Adhikary, S; Kocieda, VP; Yen, JH; Tuma, RF; Ganea, D
  • CB2-receptor stimulation attenuates TNF-α-induced human endothelial cell activation, transendothelial migration of monocytes, and monocyte-endothelial adhesion
    Rajesh, M; Mukhopadhyay, P; Batkai, S; Hasko, G; Liaudet, L; Huffman, JW; Csiszar, A; Ungvari, Z; Mackie, K; Chatterjee, S; Pacher, P
  • Activation of cannabinoid type two receptors (CB2) diminish inflammatory responses in macrophages and brain endothelium
    Persidsky, Y; Fan, S; Dykstra, H; Reichenbach, NL; Rom, S; Ramirez, SH
  • The cannabinoid WIN55,212-2 protects against oxidized LDL-induced inflammatory response in murine macrophages
    Hao, MX; Jiang, LS; Fang, NY; Pu, J; Hu, LH; Shen, LH; Song, W; He, B
  • Inhibition of nitric oxide production in RAW264.7 macrophages by cannabinoids and palmitoylethanolamide
    Ross, RA; Brockie, HC; Pertwee, RG
  • The cannabinoid Δ-9-tetrahydrocannabinol mediates inhibition of macrophage chemotaxis to RANTES/CCL5: linkage to the CB2 receptor
    Raborn, ES; Marciano-Cabral, F; Buckley, NE; Martin, BR; Cabral, GA
  • Activation of cannabinoid CB2 receptor negatively regulates IL-12p40 production in murine macrophages: role of IL-10 and ERK1/2 kinase signaling
    Correa, F; Mestre, L; Docagne, F; Guaza, C
  • Cannabidiol, unlike synthetic cannabinoids, triggers activation of RBL-2H3 mast cells
    Giudice, ED; Rinaldi, L; Passarotto, M; Facchinetti, F; D’Arrigo, A; Guiotto, A; Carbonare, MD; Battistin, L; Leon, A
  • Cannabinoid receptor type 2 activation induces a microglial anti-inflammatory phenotype and reduces migration via MKP induction and ERK dephosphorylation
    Romero-Sandoval, EA; Horvath, R; Landry, RP; DeLeo, JA
  • Activation of cannabinoid 2 receptors protects against cerebral ischemia by inhibiting neutrophil recruitment
    Murikinati, S; Juttler, E; Keinert, T; Ridder, DA; Muhammad, S; Waibler, Z; Ledent, C; Zimmer, A; Kalinke, U; Schwaninger, M
  • The activation of the cannabinoid receptor type 2 reduces neutrophilic protease-mediated vulnerability in atherosclerotic plaques
    Montecucco, F; Marzo, V; Silva, RF; Vuilleumier, N; Capettini, L; Lenglet, S; Pagano, S; Piscitelli, F; Quintao, S; Bertolotto, M; Pelli, G; Galan, K; Pilet, L; Kuzmanovic, K; Burger, F; Pane, B; Spinella, G; Braunersreuther, V; Gayet-Ageron, A; Pende, A; Viviani, GL; Palombo, D; Dallegri, F; Roux-Lombard, P; Santos, RA; Stergiopulos, N; Steffens, S; Mach, F
  • Δ9-tetrahydrocannabinol regulates Th1/Th2 cytokine balance in activated human T cells
    Yuan, M; Kiertscher, SM; Cheng, Q; Zoumalan, R; Tashkin, DP; Roth, MD
  • Cannabinoid receptor CB2 modulates the CXCL12/CXCR4-mediated chemotaxis of T lymphocytes
    Ghosh, S; Preet, A; Groopman, JE; Ganju, RK
  • A CB2-selective cannabinoid suppresses T-cell activities and increases tregs and IL-10
    Robinson, RH; Meissler, JJ; Fan, X; Yu, D; Adler, MW; Eisenstein, TK
  • CB2 cannabinoid receptors contribute to bacterial invasion and mortality in polymicrobial sepsis
    Csoka, B; Nemeth, ZH; Mukhopadhyay, P; Spolarics, Z; Rajesh, M; Federici, S; Deitch, EA; Batkai, S; Pacher, P; Hasko, G
  • Attenuation of allergic contact dermatitis through the endocannabinoid system
    Karsak, M; Gaffal, E; Date, R; Wang-Eckhardt, L; Rehnelt, J; Petrosino, S; Starowicz, K; Steuder, R; Schlicker, E; Cravatt, B; Mechoulam, R; Buettner, R; Werner, S; Marzo, V; Tuting, T; Zimmer, A
  • Attenuation of experimental autoimmune hepatitis by exogenous and endogenous cannabinoids: involvement of regulatory T cells
    Hegde, VL; Hegde, S; Cravatt, BF; Hofseth, LJ; Nagarkatti, M; Nagarkatti, PS
  • Mice lacking cannabinoid CB1-, CB2-receptors or both receptors show increased susceptibility to trinitrobenzene sulfonic acid (TNBS)-induced colitis
    Engel, MA; Kellermann, CA; Burnat, G; Hahn, EG; Rau, T; Konturek, PC
  • Impaired border zone formation and adverse remodeling after reperfused myocardial infarction in cannabinoid CB2 receptor deficient mice
    Duerr, GD; Heinemann, JC; Gestrich, C; Heuft, T; Klaas, T; Keppel, K; Roell, W; Klein, A; Zimmer, A; Velten, M; Kilic, A; Bindila, L; Lutz, B; Dewald, O
  • Cannabinoid receptor type-2 stimulation, blockade, and deletion alter the vascular inflammatory responses to traumatic brain injury
    Amenta, PS; Jallo, JI; Tuma, RF; Hooper, DC; Elliott, MB
  • WIN55212-2 ameliorates atherosclerosis associated with suppression of pro-inflammatory responses in ApoE-knockout mice
    Zhao, Y; Liu, Y; Zhang, W; Xue, J; Wu, YZ; Xu, W; Liang, X; Chen, T; Kishimoto, C; Yuan, Z
  • Low dose oral cannabinoid therapy reduces progression of atherosclerosis in mice
    Steffens, S; Veillard, NR; Arnaud, C; Pelli, G; Burger, F; Staub, C; Karsak, M; Zimmer, A; Frossard, JL; Mach, F
  • Δ-9-tetrahydrocannabinol enhances breast cancer growth and metastasis by suppression of the antitumor immune response
    McKallip, RJ; Nagarkatti, M; Nagarkatti, PS
  • Cannabinoid type 2 receptor activation downregulates stroke-induced classic and alternative brain macrophage/microglial activation concomitant to neuroprotection
    Zarruk, JG; Fernandez-Lopez, D; Garcia-Yebenes, I; Garcia-Gutierrez, MS; Vivancos, J; Nombela, F; Torres, M; Burguete, MC; Manzanares, J; Lizasoain, I; Moro, MA
  • Direct suppression of CNS autoimmune inflammation via the cannabinoid receptor CB1 on neurons and CB2 on autoreactive T cells
    Maresz, K; Pryce, G; Ponomarev, ED; Marsicano, G; Croxford, JL; Shriver, LP; Ledent, C; Cheng, X; Carrier, EJ; Mann, MK; Giovannoni, G; Pertwee, RG; Yamamura, T; Buckley, NE; Hillard, CJ; Lutz, B; Baker, D; Dittel, BN
  • Δ8-Tetrahydrocannabivarin prevents hepatic ischaemia/reperfusion injury by decreasing oxidative stress and inflammatory responses through cannabinoid CB2 receptors
    Batkai, S; Mukhopadhyay, P; Horvath, B; Rajesh, M; Gao, RY; Mahadevan, A; Amere, M; Battista, N; Lichtman, AH; Gauson, LA; Maccarrone, M; Pertwee, RG; Pacher, P
  • Minocycline attenuates neonatal germinal-matrix-hemorrhage-induced neuroinflammation and brain edema by activating cannabinoid receptor 2
    Tang, J; Chen, Q; Guo, J; Yang, L; Tao, Y; Li, L; Miao, H; Feng, H; Chen, Z; Zhu, G
  • CB1 and CB2 cannabinoid receptors mediate different aspects of Δ-9-tetrahydrocannabinol (THC)-induced T helper cell shift following immune activation by Legionella pneumophila infection
    Newton, CA; Chou, PJ; Perkins, I; Klein, TW
  • Targeted deletion of cannabinoid receptors CB1 and CB2 produced enhanced inflammatory responses to influenza A/PR/8/34 in the absence and presence of Delta9-tetrahydrocannabinol
    Buchweitz, JP; Karmaus, PW; Williams, KJ; Harkema, JR; Kaminski, NE
  • Cannabinoid CB2 receptor activation reduces mouse myocardial ischemia-reperfusion injury: involvement of cytokine/chemokines and PMN
    Filippo, C; Rossi, F; Rossi, S; D’Amico, M
  • Activation of cannabinoid receptors prevents antigen-induced asthma-like reaction in guinea pigs
    Giannini, L; Nistri, S; Mastroianni, R; Cinci, L; Vannacci, A; Mariottini, C; Passani, MB; Mannaioni, PF; Bani, D; Masini, E
  • Evaluation of selective cannabinoid CB1 and CB2 receptor agonists in a mouse model of lipopolysaccharide-induced interstitial cystitis
    Tambaro, S; Casu, MA; Mastinu, A; Lazzari, P
  • Experimental cannabinoid 2 receptor-mediated immune modulation in sepsis
    Sardinha, J; Kelly, ME; Zhou, J; Lehmann, C
  • Modulation of inflammatory responses by a cannabinoid-2-selective agonist after spinal cord injury
    Adhikary, S; Li, H; Heller, J; Skarica, M; Zhang, M; Ganea, D; Tuma, RF
  • Regulatory role of the cannabinoid CB2 receptor in stress-induced neuroinflammation in mice
    Zoppi, S; Madrigal, JL; Caso, JR; Garcia-Gutierrez, MS; Manzanares, J; Leza, JC; Garcia-Bueno, B
  • A cannabinoid type 2 receptor agonist attenuates blood-brain barrier damage and neurodegeneration in a murine model of traumatic brain injury
    Amenta, PS; Jallo, JI; Tuma, RF; Elliott, MB
  • Brain monoglyceride lipase participating in endocannabinoid inactivation
    Dinh, TP; Carpenter, D; Leslie, FM; Freund, TF; Katona, I; Sensi, SL; Kathuria, S; Piomelli, D
  • Anandamide amidohydrolase reacting with 2-arachidonoylglycerol, another cannabinoid receptor ligand
    Goparaju, SK; Ueda, N; Yamaguchi, H; Yamamoto, S
  • Endocannabinoid oxygenation by cyclooxygenases, lipoxygenases, and cytochromes P450: cross-talk between the eicosanoid and endocannabinoid signaling pathways
    Rouzer, CA; Marnett, LJ
  • The inhibition of monoacylglycerol lipase by URB602 showed an anti-inflammatory and anti-nociceptive effect in a murine model of acute inflammation
    Comelli, F; Giagnoni, G; Bettoni, I; Colleoni, M; Costa, B
  • Activation of CB2 receptor is required for the therapeutic effect of ABHD6 inhibition in experimental autoimmune encephalomyelitis
    Wen, J; Ribeiro, R; Tanaka, M; Zhang, Y
  • Monoacylglycerol lipase (MAGL) inhibition attenuates acute lung injury in mice
    Costola-de-Souza, C; Ribeiro, A; Ferraz-de-Paula, V; Calefi, AS; Aloia, TP; Gimenes-Junior, JA; Almeida, VI; Pinheiro, ML; Palermo-Neto, J
  • Regulation of inflammatory pain by inhibition of fatty acid amide hydrolase
    Naidu, PS; Kinsey, SG; Guo, TL; Cravatt, BF; Lichtman, AH
  • The fatty acid amide hydrolase (FAAH) inhibitor PF-3845 acts in the nervous system to reverse LPS-induced tactile allodynia in mice
    Booker, L; Kinsey, SG; Abdullah, RA; Blankman, JL; Long, JZ; Ezzili, C; Boger, DL; Cravatt, BF; Lichtman, AH
  • Tapping into the endocannabinoid system to ameliorate acute inflammatory flares and associated pain in mouse knee joints
    Krustev, E; Reid, A; McDougall, JJ
  • Increasing endogenous 2-arachidonoylglycerol levels counteracts colitis and related systemic inflammation
    Alhouayek, M; Lambert, DM; Delzenne, NM; Cani, PD; Muccioli, GG
  • Anticoagulant albumin fragments that bind to fibrinogen/fibrin: possible implications
    Galanakis, DK
  • Involvement of the cannabinoid CB2 receptor and its endogenous ligand 2-arachidonoylglycerol in oxazolone-induced contact dermatitis in mice
    Oka, S; Wakui, J; Ikeda, S; Yanagimoto, S; Kishimoto, S; Gokoh, M; Nasui, M; Sugiura, T
  • Modulation of the cannabinoid CB2 receptor in microglial cells in response to inflammatory stimuli
    Maresz, K; Carrier, EJ; Ponomarev, ED; Hillard, CJ; Dittel, BN
  • COX-2, CB2 and P2X7-immunoreactivities are increased in activated microglial cells/macrophages of multiple sclerosis and amyotrophic lateral sclerosis spinal cord
    Yiangou, Y; Facer, P; Durrenberger, P; Chessell, IP; Naylor, A; Bountra, C; Banati, RR; Anand, P
  • Behavioral, pharmacological and molecular characterization of the saphenous nerve partial ligation: a new model of neuropathic pain
    Walczak, JS; Pichette, V; Leblond, F; Desbiens, K; Beaulieu, P
  • Evidence for the involvement of the cannabinoid CB2 receptor and its endogenous ligand 2-arachidonoylglycerol in 12-O-tetradecanoylphorbol-13-acetate-induced acute inflammation in mouse ear
    Oka, S; Yanagimoto, S; Ikeda, S; Gokoh, M; Kishimoto, S; Waku, K; Ishima, Y; Sugiura, T
  • Rheumatoid arthritis. Pathophysiology and implications for therapy
    Harris, ED
  • Characterisation of the cannabinoid receptor system in synovial tissue and fluid in patients with osteoarthritis and rheumatoid arthritis
    Richardson, D; Pearson, RG; Kurian, N; Latif, ML; Garle, MJ; Barrett, DA; Kendall, DA; Scammell, BE; Reeve, AJ; Chapman, V
  • Expression of cannabinoid receptor 2 and its inhibitory effects on synovial fibroblasts in rheumatoid arthritis
    Gui, H; Liu, X; Wang, ZW; He, DY; Su, DF; Dai, SM
  • Cannabinoid receptor 2 as a potential therapeutic target in rheumatoid arthritis
    Fukuda, S; Kohsaka, H; Takayasu, A; Yokoyama, W; Miyabe, C; Miyabe, Y; Harigai, M; Miyasaka, N; Nanki, T
  • The type 2 cannabinoid receptor regulates bone mass and ovariectomy-induced bone loss by affecting osteoblast differentiation and bone formation
    Sophocleous, A; Landao-Bassonga, E; Van’t Hof, RJ; Idris, AI; Ralston, SH
  • Activation of cannabinoid receptor 2 attenuates synovitis and joint distruction in collagen-induced arthritis
    Gui, H; Liu, X; Liu, LR; Su, DF; Dai, SM
  • A novel synthetic, nonpsychoactive cannabinoid acid (HU-320) with antiinflammatory properties in murine collagen-induced arthritis
    Sumariwalla, PF; Gallily, R; Tchilibon, S; Fride, E; Mechoulam, R; Feldmann, M
  • The pathology of atherosclerosis: plaque development and plaque responses to medical treatment
    Insull, W
  • Detailed characterization of the endocannabinoid system in human macrophages and foam cells, and anti-inflammatory role of type-2 cannabinoid receptor
    Chiurchiu, V; Lanuti, M; Catanzaro, G; Fezza, F; Rapino, C; Maccarrone, M
  • Activation of cannabinoid CB2 receptor ameliorates atherosclerosis associated with suppression of adhesion molecules
    Zhao, Y; Yuan, Z; Liu, Y; Xue, J; Tian, Y; Liu, W; Zhang, W; Shen, Y; Xu, W; Liang, X; Chen, T
  • Cannabinoid receptor type 2 (CB2) deficiency alters atherosclerotic lesion formation in hyperlipidemic Ldlr-null mice
    Netherland, CD; Pickle, TG; Bales, A; Thewke, DP
  • Cannabinoid receptor 2 deficiency in haematopoietic cells aggravates early atherosclerosis in LDL receptor deficient mice
    Delsing, DJ; Leijten, FP; Arts, K; Eenennaam, H; Garritsen, A; Gijbels, MJ; Winther, MP; Elsas, A
  • Cannabinoid receptor type 2 (CB2) dependent and independent effects of WIN55,212-2 on atherosclerosis in Ldlr-null mice
    Netherland-Van Dyke, C; Rodgers, W; Fulmer, M; Lahr, Z; Thewke, D
  • Cannabinoid receptor 2 signaling does not modulate atherogenesis in mice
    Willecke, F; Zeschky, K; Ortiz Rodriguez, A; Colberg, C; Auwarter, V; Kneisel, S; Hutter, M; Lozhkin, A; Hoppe, N; Wolf, D; Muhlen, C; Moser, M; Hilgendorf, I; Bode, C; Zirlik, A
  • Inflammatory bowel disease: epidemiology, pathogenesis, and therapeutic opportunities
    Hanauer, SB
  • The endogenous cannabinoid system protects against colonic inflammation
    Massa, F; Marsicano, G; Hermann, H; Cannich, A; Monory, K; Cravatt, BF; Ferri, GL; Sibaev, A; Storr, M; Lutz, B
  • Targeting endocannabinoid degradation protects against experimental colitis in mice: involvement of CB1 and CB2 receptors
    Storr, MA; Keenan, CM; Emmerdinger, D; Zhang, H; Yuce, B; Sibaev, A; Massa, F; Buckley, NE; Lutz, B; Goke, B; Brand, S; Patel, KD; Sharkey, KA
  • Activation of the cannabinoid 2 receptor (CB2) protects against experimental colitis
    Storr, MA; Keenan, CM; Zhang, H; Patel, KD; Makriyannis, A; Sharkey, KA
  • Beneficial effect of the non-psychotropic plant cannabinoid cannabigerol on experimental inflammatory bowel disease
    Borrelli, F; Fasolino, I; Romano, B; Capasso, R; Maiello, F; Coppola, D; Orlando, P; Battista, G; Pagano, E; Marzo, V; Izzo, AA
  • β-caryophyllene inhibits dextran sulfate sodium-induced colitis in mice through CB2 receptor activation and PPARγ pathway
    Bento, AF; Marcon, R; Dutra, RC; Claudino, RF; Cola, M; Leite, DF; Calixto, JB
  • 4-Oxo-1,4-Dihydropyridines as selective CB(2) cannabinoid receptor ligands. Part 2: discovery of new agonists endowed with protective effect against experimental colitis
    Bakali, J; Gilleron, P; Body-Malapel, M; Mansouri, R; Muccioli, GG; Djouina, M; Barczyk, A; Klupsch, F; Andrzejak, V; Lipka, E; Furman, C; Lambert, DM; Chavatte, P; Desreumaux, P; Millet, R
  • 3-Carboxamido-5-aryl-isoxazoles as new CB2 agonists for the treatment of colitis
    Tourteau, A; Andrzejak, V; Body-Malapel, M; Lemaire, L; Lemoine, A; Mansouri, R; Djouina, M; Renault, N; Bakali, J; Desreumaux, P; Muccioli, GG; Lambert, DM; Chavatte, P; Rigo, B; Leleu-Chavain, N; Millet, R
  • Conformational restriction leading to a selective CB2 cannabinoid receptor agonist orally active against colitis
    Bakali, J; Muccioli, GG; Body-Malapel, M; Djouina, M; Klupsch, F; Ghinet, A; Barczyk, A; Renault, N; Chavatte, P; Desreumaux, P; Lambert, DM; Millet, R
  • Discovery of 2-[(2,4-dichlorophenyl)amino]-N-[(tetrahydro- 2H-pyran-4-yl)methyl]-4-(trifluoromethyl)-5-pyrimidinecarboxamide, a selective CB2 receptor agonist for the treatment of inflammatory pain
    Giblin, GM; O’Shaughnessy, CT; Naylor, A; Mitchell, WL; Eatherton, AJ; Slingsby, BP; Rawlings, DA; Goldsmith, P; Brown, AJ; Haslam, CP; Clayton, NM; Wilson, AW; Chessell, IP; Wittington, AR; Green, R
  • Pyridine-3-carboxamides as novel CB2 agonists for analgesia
    Mitchell, WL; Giblin, GM; Naylor, A; Eatherton, AJ; Slingsby, BP; Rawlings, AD; Jandu, KS; Haslam, CP; Brown, AJ; Goldsmith, P; Clayton, NM; Wilson, AW; Chessell, IP; Green, RH; Whittington, AR; Wall, ID
  • Discovery of 1-[4-(3-chlorophenylamino)-1-methyl-1H-pyrrolo[3,2-c]pyridin-7-yl]-1-morpholin-4-ylmethanone (GSK554418A), a brain penetrant 5-azaindole CB2 agonist for the treatment of chronic pain
    Giblin, GM; Billinton, A; Briggs, M; Brown, AJ; Chessell, IP; Clayton, NM; Eatherton, AJ; Goldsmith, P; Haslam, C; Johnson, MR; Mitchell, WL; Naylor, A; Perboni, A; Slingsby, BP; Wilson, AW