The role of cannabinoid receptors and the endocannabinoid system in mantle cell lymphoma and other non-Hodgkin lymphomas

Seminars in Cancer Biology

Volumn 21, Issue 5, 2011, Pages 313-321

  Wasik, Agata M ^a   Christensson, Birger ^a   Sander, Birgitta ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Apoptosis; Cannabinoid receptors; Mantle cell lymphoma; Non Hodgkin lymphoma; Paraptosis; Programmed cell death

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 5 (4 CHLORO 3 METHYLPHENYL) 1 (4 METHYLBENZYL) N (1,3,3 TRIMETHYLBICYCLO[2.2.1]HEPTAN 2 YL) 3 PYRAZOLECARBOXAMIDE; ANANDAMIDE; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR; CASPASE 3; CD40 ANTIGEN; ENDOCANNABINOID; FATTY ACID AMIDASE; INTERLEUKIN 4; METHANANDAMIDE; PROTEIN KINASE SYK; RIMONABANT; TRANSCRIPTION FACTOR SOX11;

APOPTOSIS; B CELL LYMPHOMA; B LYMPHOCYTE; CELL CYCLE ARREST; CELL MIGRATION; CELL PROLIFERATION; CYTOKINE PRODUCTION; EATING DISORDER; ENDOPLASMIC RETICULUM STRESS; FOLLICULAR LYMPHOMA; GENE EXPRESSION; HUMAN; INTERNALIZATION; LARGE CELL LYMPHOMA; LYMPHOCYTOMA; MANTLE CELL LYMPHOMA; NONHODGKIN LYMPHOMA; NONHUMAN; OBESITY; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; REVIEW; T LYMPHOCYTE; TRANSCRIPTION REGULATION; UPREGULATION;

CANNABINOID RECEPTOR MODULATORS; ENDOCANNABINOIDS; HUMANS; LYMPHOMA, MANTLE-CELL; LYMPHOMA, NON-HODGKIN; RECEPTORS, CANNABINOID;

EID: 82555187101     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2011.10.004     Document Type: Review

References (103)

1. Perez-Galan P., Dreyling M., Wiestner A. Mantle cell lymphoma: biology, pathogenesis, and the molecular basis of treatment in the genomic era. Blood 2011, 117(1):26-38.
2. Stamatopoulos K., Kosmas C., Belessi C., Kyriazopoulos P., Papadaki T., Anagnostou D., et al. Molecular analysis of bcl-1/IgH junctional sequences in mantle cell lymphoma: potential mechanism of the t(11;14) chromosomal translocation. Br J Haematol 1999, 105(1):190-197.
3. Hadzidimitriou A., Agathangelidis A., Darzentas N., Murray F., Delfau-Larue M.H., Bredo Pedersen L., et al. Is there a role for antigen selection in mantle cell lymphoma? Immunogenetic support from a series of 807 cases. Blood 2011, 118(11):3088-3095.
4. Kolar G.R., Mehta D., Pelayo R., Capra J.D. A novel human B cell subpopulation representing the initial germinal center population to express AID. Blood 2007, 109(6):2545-2552.
5. Ek S., Hogerkorp C.M., Dictor M., Ehinger M., Borrebaeck C.A. Mantle cell lymphomas express a distinct genetic signature affecting lymphocyte trafficking and growth regulation as compared with subpopulations of normal human B cells. Cancer Res 2002, 62(15):4398-4405.
6. Islam T.C., Asplund A.C., Lindvall J.M., Nygren L., Liden J., Kimby E., et al. High level of cannabinoid receptor 1, absence of regulator of G protein signalling 13 and differential expression of Cyclin D1 in mantle cell lymphoma. Leukemia 2003, 17(9):1880-1890.
7. Gustafsson K., Wang X., Severa D., Eriksson M., Kimby E., Merup M., et al. Expression of cannabinoid receptors type 1 and type 2 in non-Hodgkin lymphoma: growth inhibition by receptor activation. Int J Cancer 2008, 123(5):1025-1033.
8. Harkany T., Mackie K., Doherty P. Wiring and firing neuronal networks: endocannabinoids take center stage. Curr Opin Neurobiol 2008, 18(3):338-345.
9. Cabral G.A., Griffin-Thomas L. Emerging role of the cannabinoid receptor CB2 in immune regulation: therapeutic prospects for neuroinflammation. Expert Rev Mol Med 2009, 11:e3.
10. Miller A.M., Stella N. CB2 receptor-mediated migration of immune cells: it can go either way. Br J Pharmacol 2008, 153(2):299-308.
11. Ziring D., Wei B., Velazquez P., Schrage M., Buckley N.E., Braun J. Formation of B and T cell subsets require the cannabinoid receptor CB2. Immunogenetics 2006, 58(9):714-725.
12. Matsuda L.A., Lolait S.J., Brownstein M.J., Young A.C., Bonner T.I. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990, 346(6284):561-564.
13. Munro S., Thomas K.L., Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993, 365(6441):61-65.
14. Jorda M.A., Lowenberg B., Delwel R. The peripheral cannabinoid receptor Cb2, a novel oncoprotein, induces a reversible block in neutrophilic differentiation. Blood 2003, 101(4):1336-1343.
15. Howlett A.C., Qualy J.M., Khachatrian L.L. Involvement of Gi in the inhibition of adenylate cyclase by cannabimimetic drugs. Mol Pharmacol 1986, 29(3):307-313.
16. Hudson B.D., Hebert T.E., Kelly M.E. Ligand- and heterodimer-directed signaling of the CB (1) cannabinoid receptor. Mol Pharmacol 2010, 77(1):1-9.
17. Ross R.A. Anandamide and vanilloid TRPV1 receptors. Br J Pharmacol 2003, 140(5):790-801.
18. Sharir H., Abood M.E. Pharmacological characterization of GPR55, a putative cannabinoid receptor. Pharmacol Ther 2010, 126(3):301-313.
19. Pertwee R.G., Howlett A.C., Abood M.E., Alexander S.P., Di Marzo V., Elphick M.R., et al. International Union of Basic and Clinical Pharmacology. LXXIX. Cannabinoid receptors and their ligands: beyond CB and CB. Pharmacol Rev 2010, 62(4):588-631.
20. O'Sullivan S.E. Cannabinoids go nuclear: evidence for activation of peroxisome proliferator-activated receptors. Br J Pharmacol 2007, 152(5):576-582.
21. Klein T.W., Newton C., Larsen K., Lu L., Perkins I., Nong L., et al. The cannabinoid system and immune modulation. J Leukoc Biol 2003, 74(4):486-496.
22. Waldeck-Weiermair M., Zoratti C., Osibow K., Balenga N., Goessnitzer E., Waldhoer M., et al. Integrin clustering enables anandamide-induced Ca2+ signaling in endothelial cells via GPR55 by protection against CB1-receptor-triggered repression. J Cell Sci 2008, 121(Pt 10):1704-1717.
23. Waldeck-Weiermair M., Zoratti C., Osibow K., Balenga N., Goessnitzer E., Waldhoer M., et al. Genomic and expression profiling identifies the B-cell associated tyrosine kinase Syk as a possible therapeutic target in mantle cell lymphoma. Br J Haematol 2006, 132(3):303-316.
24. McIntosh H.H., Song C., Howlett A.C. CB1 cannabinoid receptor: cellular regulation and distribution in N18TG2 neuroblastoma cells. Brain Res Mol Brain Res 1998, 53(1-2):163-173.
25. Rozenfeld R., Devi L.A. Regulation of CB1 cannabinoid receptor trafficking by the adaptor protein AP-3. FASEB J 2008, 22(7):2311-2322.
26. Grimsey N.L., Graham E.S., Dragunow M., Glass M. Cannabinoid Receptor 1 trafficking and the role of the intracellular pool: implications for therapeutics. Biochem Pharmacol 2010, 80(7):1050-1062.
27. Brailoiu G.C., Oprea T.I., Zhao P., Abood M.E., Brailoiu E. Intracellular cannabinoid type 1 (CB1) receptors are activated by anandamide. J Biol Chem 2011, 286(33):29166-29174.
28. Devane W.A., Hanus L., Breuer A., Pertwee R.G., Stevenson L.A., Griffin G., et al. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 1992, 258(5090):1946-1949.
29. Mechoulam R., Ben-Shabat S., Hanus L., Ligumsky M., Kaminski N.E., Schatz A.R., et al. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 1995, 50(1):83-90.
30. Hanus L., Abu-Lafi S., Fride E., Breuer A., Vogel Z., Shalev D.E., et al. 2-arachidonyl glyceryl ether, an endogenous agonist of the cannabinoid CB1 receptor. Proc Natl Acad Sci USA 2001, 98(7):3662-3665.
31. Porter A.C., Sauer J.M., Knierman M.D., Becker G.W., Berna M.J., Bao J., et al. Characterization of a novel endocannabinoid, virodhamine, with antagonist activity at the CB1 receptor. J Pharmacol Exp Ther 2002, 301(3):1020-1024.
32. Bisogno T., Maurelli S., Melck D., De Petrocellis L., Di Marzo V. Biosynthesis, uptake, and degradation of anandamide and palmitoylethanolamide in leukocytes. J Biol Chem 1997, 272(6):3315-3323.
33. Centonze D., Bari M., Rossi S., Prosperetti C., Furlan R., Fezza F., et al. The endocannabinoid system is dysregulated in multiple sclerosis and in experimental autoimmune encephalomyelitis. Brain: J Neurol 2007, 130(Pt 10):2543-2553.
34. Felder C.C., Nielsen A., Briley E.M., Palkovits M., Priller J., Axelrod J., et al. Isolation and measurement of the endogenous cannabinoid receptor agonist, anandamide, in brain and peripheral tissues of human and rat. FEBS Lett 1996, 393(2-3):231-235.
35. Wagner J.A., Varga K., Ellis E.F., Rzigalinski B.A., Martin B.R., Kunos G. Activation of peripheral CB1 cannabinoid receptors in haemorrhagic shock. Nature 1997, 390(6659):518-521.
36. Varga K., Wagner J.A., Bridgen D.T., Kunos G. Platelet- and macrophage-derived endogenous cannabinoids are involved in endotoxin-induced hypotension. FASEB J 1998, 12(11):1035-1044.
37. De Petrocellis L., Melck D., Bisogno T., Di Marzo V. Endocannabinoids and fatty acid amides in cancer, inflammation and related disorders. Chem Phys Lipids 2000, 108(1-2):191-209.
38. Bojesen I.N, Hansen H.S. Binding of anandamide to bovine serum albumin. J Lipid Res 2003, 44(9):1790-1794.
39. Oddi S., Fezza F., Pasquariello N., D'Agostino A., Catanzaro G., De Simone C., et al. Molecular identification of albumin and Hsp70 as cytosolic anandamide-binding proteins. Chem Biol 2009, 16(6):624-632.
40. Kaczocha M., Glaser S.T., Deutsch D.G. Identification of intracellular carriers for the endocannabinoid anandamide. Proc Natl Acad Sci USA 2009, 106(15):6375-6380.
41. Rinaldi-Carmona M., Barth F., Heaulme M., Shire D., Calandra B., Congy C., et al. SR141716A, a potent and selective antagonist of the brain cannabinoid receptor. FEBS Lett 1994, 350(2-3):240-244.
42. Rinaldi-Carmona M., Barth F., Millan J., Derocq J.M., Casellas P., Congy C., et al. SR144528, the first potent and selective antagonist of the CB2 cannabinoid receptor. J Pharmacol Exp Ther 1998, 284(2):644-650.
43. Di Marzo V. Targeting the endocannabinoid system: to enhance or reduce?. Nat Rev Drug Discov 2008, 7(5):438-455.
44. Minkkila A., Saario S., Nevalainen T. Discovery and development of endocannabinoid-hydrolyzing enzyme inhibitors. Curr Top Med Chem 2010, 10(8):828-858.
45. Richardson S.J., Widmer M., Zajicek J., Rule S.A. Physiological doses of cannabinoids do not adversely affect MCL viability. Leuk Lymphoma 2007, 48(9):1855-1857.
46. Fernandez V., Salamero O., Espinet B., Sole F., Royo C., Navarro A., et al. Genomic and gene expression profiling defines indolent forms of mantle cell lymphoma. Cancer Res 2010, 70(4):1408-1418.
47. Galiegue S., Mary S., Marchand J., Dussossoy D., Carriere D., Carayon P., et al. Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. Eur J Biochem 1995, 232(1):54-61.
48. Bouaboula M., Rinaldi M., Carayon P., Carillon C., Delpech B., Shire D., et al. Cannabinoid-receptor expression in human leukocytes. Eur J Biochem 1993, 214(1):173-180.
49. Ek S., Dictor M., Jerkeman M., Jirstrom K., Borrebaeck C.A. Nuclear expression of the non B-cell lineage Sox11 transcription factor identifies mantle cell lymphoma. Blood 2008, 111(2):800-805.
50. Wang X., Asplund A.C., Porwit A., Flygare J., Smith C.I., Christensson B., Sander B. The subcellular Sox11 distribution pattern identifies subsets of mantle cell lymphoma: correlation to overall survival. Br J Haematol 2008, 143(2):248-252.
51. Wang X., Bjorklund S., Wasik A.M., Grandien A., Andersson P., Kimby E., et al. Gene expression profiling and chromatin immunoprecipitation identify DBN1, SETMAR and HIG2 as direct targets of SOX11 in mantle cell lymphoma. PLoS One 2010, 5(11.):e14085.
52. Wasik AM, Almestrand S, Wang X, Hultenby K, Dackland Å-L, Andersson P, Kimby E, Christensson B, Sander B. WIN55,212-2 induces cytoplasmic vacuolation in apotosis-resistant MCL cells. Cell Death and Disease (2011) 2, eK; doi:10.1038/cddis.2011.106.
53. Flygare J., Gustafsson K., Kimby E., Christensson B., Sander B. Cannabinoid receptor ligands mediate growth inhibition and cell death in mantle cell lymphoma. FEBS Lett 2005, 579(30):6885-6889.
54. Gustafsson K., Christensson B., Sander B., Flygare J. Cannabinoid receptor-mediated apoptosis induced by R(+)-methanandamide and Win55,212-2 is associated with ceramide accumulation and p38 activation in mantle cell lymphoma. Mol Pharmacol 2006, 70(5):1612-1620.
55. Herrera B., Carracedo A., Diez-Zaera M., Guzman M., Velasco G. p38 MAPK is involved in CB2 receptor-induced apoptosis of human leukaemia cells. FEBS Lett 2005, 579(22):5084-5088.
56. McKallip R.J., Lombard C., Fisher M., Martin B.R., Ryu S., Grant S., et al. Targeting CB2 cannabinoid receptors as a novel therapy to treat malignant lymphoblastic disease. Blood 2002, 100(2):627-634.
57. McKallip R.J., Jia W., Schlomer J., Warren J.W., Nagarkatti P.S., Nagarkatti M. Cannabidiol-induced apoptosis in human leukemia cells: a novel role of cannabidiol in the regulation of p22phox and Nox4 expression. Mol Pharmacol 2006, 70(3):897-908.
58. Velasco G., Galve-Roperh I., Sanchez C., Blazquez C., Haro A., Guzman M. Cannabinoids and ceramide: two lipids acting hand-by-hand. Life Sci 2005, 77(14):1723-1731.
59. Ogretmen B., Hannun Y.A. Biologically active sphingolipids in cancer pathogenesis and treatment. Nat Rev Cancer 2004, 4(8):604-616.
60. Carracedo A., Gironella M., Lorente M., Garcia S., Guzman M., Velasco G., et al. Cannabinoids induce apoptosis of pancreatic tumor cells via endoplasmic reticulum stress-related genes. Cancer Res 2006, 66(13):6748-6755.
61. Carracedo A., Lorente M., Egia A., Blazquez C., Garcia S., Giroux V., et al. The stress-regulated protein p8 mediates cannabinoid-induced apoptosis of tumor cells. Cancer Cell 2006, 9(4):301-312.
62. Chanda D., Kim D.K., Li T., Kim Y.H., Koo S.H., Lee C.H., et al. Cannabinoid receptor type 1 (CB1R) signaling regulates hepatic gluconeogenesis via induction of endoplasmic reticulum-bound transcription factor cAMP-responsive element-binding protein H (CREBH) in primary hepatocytes. J Biol Chem 2011, 286(32):27971-27979.
63. Thomas K.C., Sabnis A.S., Johansen M.E., Lanza D.L., Moos P.J., Yost G.S., et al. Transient receptor potential vanilloid 1 agonists cause endoplasmic reticulum stress and cell death in human lung cells. J Pharmacol Exp Ther 2007, 321(3):830-838.
64. Lim J.C., Lim S.K., Park M.J., Kim G.Y., Han H.J., Park S.H. Cannabinoid receptor 1 mediates high glucose-induced apoptosis via endoplasmic reticulum stress in primary cultured rat mesangial cells. Am J Physiol Renal Physiol 2011, 301(1):F179-F188.
65. Shrivastava A., Kuzontkoski P.M., Groopman J.E., Prasad A. Cannabidiol induces programmed cell death in breast cancer cells by coordinating the cross-talk between apoptosis and autophagy. Mol Cancer Ther 2011, 10(7):1161-1172.
66. Salazar M., Carracedo A., Salanueva I.J., Hernandez-Tiedra S., Lorente M., Egia A., et al. Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells. J Clin Investig 2009, 119(5):1359-1372.
67. Christopoulou F.D., Kiortsis D.N. An overview of the metabolic effects of rimonabant in randomized controlled trials: potential for other cannabinoid 1 receptor blockers in obesity. J Clin Pharm Ther 2011, 36(1):10-18.
68. Di Marzo V., Despres J.P. CB1 antagonists for obesity-what lessons have we learned from rimonabant?. Nat Rev Endocrinol 2009, 5(11):633-638.
69. Malfitano A.M., Laezza C., Pisanti S., Gazzerro P., Bifulco M. Rimonabant (SR141716) exerts anti-proliferative and immunomodulatory effects in human peripheral blood mononuclear cells. Br J Pharmacol 2008, 153(5):1003-1010.
70. Gustafsson K., Sander B., Bielawski J., Hannun Y.A., Flygare J. Potentiation of cannabinoid-induced cytotoxicity in mantle cell lymphoma through modulation of ceramide metabolism. Mol Cancer Res 2009, 7(7):1086-1098.
71. Rayman N., Lam K.H., Van Leeuwen J., Mulder A.H., Budel L.M., Lowenberg B., et al. The expression of the peripheral cannabinoid receptor on cells of the immune system and non-Hodgkin's lymphomas. Leuk Lymphoma 2007, 48(7):1389-1399.
72. Rayman N., Lam K.H., Laman J.D., Simons P.J., Lowenberg B., Sonneveld P., et al. Distinct expression profiles of the peripheral cannabinoid receptor in lymphoid tissues depending on receptor activation status. J Immunol 2004, 172(4):2111-2117.
73. Rayman N., Lam K.H., van der Holt B., Koss C., van Leeuwen J., Budel L.M., et al. The expression of the peripheral cannabinoid receptor CB2 has no effect on clinical outcome in diffuse large B-cell lymphomas. Eur J Haematol 2011.
74. Tagawa H., Tsuzuki S., Suzuki R., Karnan S., Ota A., Kameoka Y., et al. Genome-wide array-based comparative genomic hybridization of diffuse large B-cell lymphoma: comparison between CD5-positive and CD5-negative cases. Cancer Res 2004, 64(17):5948-5955.
75. Flygare J., Sander B. The endocannabinoid system in cancer-potential therapeutic target?. Semin Cancer Biol 2007.
76. Klein T.W., Cabral G.A. Cannabinoid-induced immune suppression and modulation of antigen-presenting cells. J Neuroimmune Pharmacol Off J Soc NeuroImmune Pharmacol 2006, 1(1):50-64.
77. Ligresti A., Bisogno T., Matias I., De Petrocellis L., Cascio M.G., Cosenza V., et al. Possible endocannabinoid control of colorectal cancer growth. Gastroenterology 2003, 125(3):677-687.
78. Graham E.S., Ball N., Scotter E.L., Narayan P., Dragunow M., Glass M. Induction of Krox-24 by endogenous cannabinoid type 1 receptors in Neuro2A cells is mediated by the MEK-ERK MAPK pathway and is suppressed by the phosphatidylinositol 3-kinase pathway. J Biol Chem 2006, 281(39):29085-29095.
79. Heimann A.S., Gomes I., Dale C.S., Pagano R.L., Gupta A., de Souza L.L., et al. Hemopressin is an inverse agonist of CB1 cannabinoid receptors. Proc Natl Acad Sci USA 2007, 104(51):20588-20593.
80. Di Marzo V., Bifulco M., De Petrocellis L. The endocannabinoid system and its therapeutic exploitation. Nat Rev Drug Discov 2004, 3(9):771-784.
81. Wiig H., Gyenge C.C., Tenstad O. The interstitial distribution of macromolecules in rat tumours is influenced by the negatively charged matrix components. J Physiol 2005, 567(Pt 2):557-567.
82. Tanasescu R., Constantinescu C.S. Cannabinoids and the immune system: an overview. Immunobiology 2010, 215(8):588-597.
83. Klein T.W. Cannabinoid-based drugs as anti-inflammatory therapeutics. Nat Rev Immunol 2005, 5(5):400-411.
84. Jorda M.A., Verbakel S.E., Valk P.J., Vankan-Berkhoudt Y.V., Maccarrone M., Finazzi-Agro A., et al. Hematopoietic cells expressing the peripheral cannabinoid receptor migrate in response to the endocannabinoid 2-arachidonoylglycerol. Blood 2002, 99(8):2786-2793.
85. Pereira J.P., An J., Xu Y., Huang Y., Cyster J.G. Cannabinoid receptor 2 mediates the retention of immature B cells in bone marrow sinusoids. Nat Immunol 2009, 10(4):403-411.
86. Muppidi J.R., Arnon T.I., Bronevetsky Y., Veerapen N., Tanaka M., Besra G.S., et al. Cannabinoid receptor 2 positions and retains marginal zone B cells within the splenic marginal zone. J Exp Med 2011, 208(10):1941-1948.
87. Carayon P., Marchand J., Dussossoy D., Derocq J.M., Jbilo O., Bord A., et al. Modulation and functional involvement of CB2 peripheral cannabinoid receptors during B-cell differentiation. Blood 1998, 92(10):3605-3615.
88. Derocq J.M., Segui M., Marchand J., Le Fur G., Casellas P. Cannabinoids enhance human B-cell growth at low nanomolar concentrations. FEBS Lett 1995, 369(2-3):177-182.
89. Schwarz H., Blanco F.J., Lotz M. Anadamide, an endogenous cannabinoid receptor agonist inhibits lymphocyte proliferation and induces apoptosis. J Neuroimmunol 1994, 55(1):107-115.
90. Noe S.N., Newton C., Widen R., Friedman H., Klein T.W. Anti-CD40, anti-CD3, and IL-2 stimulation induce contrasting changes in CB1 mRNA expression in mouse splenocytes. J Neuroimmunol 2000, 110(1-2):161-167.
91. Coopman K., Smith L.D., Wright K.L., Ward S.G. Temporal variation in CB2R levels following T lymphocyte activation: evidence that cannabinoids modulate CXCL12-induced chemotaxis. Int Immunopharmacol 2007, 7(3):360-371.
92. Borner C., Hollt V., Sebald W., Kraus J. Transcriptional regulation of the cannabinoid receptor type 1 gene in T cells by cannabinoids. J Leukoc Biol 2007, 81(1):336-343.
93. Borner C., Bedini A., Hollt V., Kraus J. Analysis of promoter regions regulating basal and interleukin-4-inducible expression of the human CB1 receptor gene in T lymphocytes. Mol Pharmacol 2008, 73(3):1013-1019.
94. Borner C., Smida M., Hollt V., Schraven B., Kraus J. Cannabinoid receptor type 1- and 2-mediated increase in cyclic AMP inhibits T cell receptor-triggered signaling. J Biol Chem 2009, 284(51):35450-35460.
95. Klein T.W., Newton C., Zhu W., Daaka Y., Friedman H. delta 9-Tetrahydrocannabinol, cytokines, and immunity to Legionella pneumophila. Proc Soc Exp Biol Med 1995, 209(3):205-212.
96. Kaplan B.L., Ouyang Y., Herring A., Yea S.S., Razdan R., Kaminski N.E. Inhibition of leukocyte function and interleukin-2 gene expression by 2-methylarachidonyl-(2'-fluoroethyl)amide, a stable congener of the endogenous cannabinoid receptor ligand anandamide. Toxicol Appl Pharmacol 2005, 205(2):107-115.
97. Cencioni M.T., Chiurchiu V., Catanzaro G., Borsellino G., Bernardi G., Battistini L., et al. Anandamide suppresses proliferation and cytokine release from primary human T-lymphocytes mainly via CB2 receptors. PLoS One 2010, 5(1):pe8688.
98. Ribeiro A., Ferraz-de-Paula V., Pinheiro M.L., Sakai M., Costa-Pinto F.A., Palermo-Neto J. Anandamide prior to sensitization increases cell-mediated immunity in mice. Int Immunopharmacol 2010, 10(4):431-439.
99. Haabeth O.A., Lorvik K.B., Hammarstrom C., Donaldson I.M., Haraldsen G., Bogen B., et al. Inflammation driven by tumour-specific Th1 cells protects against B-cell cancer. Nat Commun 2011, 2:p240.
100. Burger J.A. Chemokines and chemokine receptors in chronic lymphocytic leukemia (CLL): from understanding the basics towards therapeutic targeting. Semin Cancer Biol 2010, 20(6):424-430.
101. Kurtova A.V., Tamayo A.T., Ford R.J., Burger J.A. Mantle cell lymphoma cells express high levels of CXCR4, CXCR5, and VLA-4 (CD49d): importance for interactions with the stromal microenvironment and specific targeting. Blood 2009, 113(19):4604-4613.
102. Ghosh S., Preet A., Groopman J.E., Ganju R.K. Cannabinoid receptor CB2 modulates the CXCL12/CXCR4-mediated chemotaxis of T lymphocytes. Mol Immunol 2006, 43(14):2169-2179.
103. Rossi B., Zenaro E., Angiari S., Ottoboni L., Bach S., Piccio L., et al. Inverse agonism of cannabinoid CB1 receptor blocks the adhesion of encephalitogenic T cells in inflamed brain venules by a protein kinase A-dependent mechanism. J Neuroimmunol 2011, 233(1-2):97-105.