Dendritic cell regulation by cannabinoid-based drugs

Pharmaceuticals

Volumn 3, Issue 8, 2010, Pages 2733-2750

  Svensson, Mattias ^a   Chen, Puran ^a   Hammarfjord, Oscar ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Cannabinoids; Dendritic cells; Immunomodulation; Inflammation; Kv channels

Indexed keywords

1 DEOXY 3 (1,1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; 2 ARACHIDONOYLGLYCEROL; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; ANANDAMIDE; CANNABIDIOL; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABINOID DERIVATIVE; DEXANABINOL; ENDOCANNABINOID; ENZYME INHIBITOR; HU 331; INTERLEUKIN 10; INTERLEUKIN 12; JHW 015; POTASSIUM CHANNEL KV1.3; POTASSIUM CHANNEL KV1.5; TETRAHYDROCANNABINOLIC ACID; UNCLASSIFIED DRUG;

AMYOTROPHIC LATERAL SCLEROSIS; ANTIGEN PRESENTING CELL; ANTIINFLAMMATORY ACTIVITY; BACTERIAL INFECTION; BREAST CANCER; CELL CYCLE REGULATION; CELL FUNCTION; CELLULAR IMMUNITY; CHRONIC INFLAMMATION; COLITIS; CYTOKINE PRODUCTION; DENDRITIC CELL; DOSE RESPONSE; DOWN REGULATION; DRUG MECHANISM; GLIOMA; HEART MUSCLE INJURY; HEART MUSCLE ISCHEMIA; HUMAN; IMMUNOMODULATION; IMMUNOREGULATION; IRRITABLE COLON; LEUKEMIA; LOW DRUG DOSE; LUNG CANCER; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; LYMPHOMA; MELANOMA; NEOPLASM; NEUROMODULATION; NONHUMAN; PANCREAS CANCER; PROSTATE CANCER; PROTEIN FUNCTION; REPERFUSION INJURY; REVIEW; TH1 CELL; TH2 CELL;

EID: 77957279326     PISSN: None     EISSN: 14248247     Source Type: Journal    
DOI: 10.3390/ph3082733     Document Type: Review

References (96)

1. Piomelli, D. The molecular logic of endocannabinoid signalling. Nat. Rev. Neurosci. 2003, 4, 873-884.
2. McAllister, S.D.; Glass, M. CB(1) and CB(2) receptor-mediated signalling: A focus on endocannabinoids. Prostaglandins Leukot Essent Fatty Acids 2002, 66, 161-171.
3. Pertwee, R.G.; Ross, R.A. Cannabinoid receptors and their ligands. Prostaglandins Leukot Essent Fatty Acids 2002, 66, 101-121.
4. Blednov, Y.A.; Stoffel, M.; Alva, H.; Harris, R.A. A pervasive mechanism for analgesia: Activation of GIRK2 channels. Proc. Natl. Acad. Sci. USA 2003, 100, 277-282.
5. Guo, J.; Ikeda, S.R. Endocannabinoids modulate N-type calcium channels and G-protein-coupled inwardly rectifying potassium channels via CB1 cannabinoid receptors heterologously expressed in mammalian neurons. Mol. Pharmacol. 2004, 65, 665-674.
6. Khasabova, I.A.; Harding-Rose, C.; Simone, D.A.; Seybold, V.S. Differential effects of CB1 and opioid agonists on two populations of adult rat dorsal root ganglion neurons. J. Neurosci. 2004, 24, 1744-1753.
7. Schweitzer, P. Cannabinoids decrease the K(+) M-current in hippocampal CA1 neurons. J. Neurosci. 2000, 20, 51-58.
8. Twitchell, W.; Brown, S.; Mackie, K., Cannabinoids inhibit N- and P/Q-type calcium channels in cultured rat hippocampal neurons. J. Neurophysiol. 1997, 78, 43-50.
9. Arevalo-Martin, A.; Vela, J.M.; Molina-Holgado, E.; Borrell, J.; Guaza, C. Therapeutic action of cannabinoids in a murine model of multiple sclerosis. J. Neurosci. 2003, 23, 2511-2516.
10. Croxford, J.L.; Miller, S.D. Immunoregulation of a viral model of multiple sclerosis using the synthetic cannabinoid R+WIN55,212. J. Clin. Invest. 2003, 111, 1231-1240.
11. Klein, T.W. Cannabinoid-based drugs as anti-inflammatory therapeutics. Nat. Rev. Immunol. 2005, 5, 400-411.
12. Reis e Sousa, C. Dendritic cells in a mature age. Nat. Rev. Immunol. 2006, 6, 476-483.
13. Cella, M.; Engering, A.; Pinet, V.; Pieters, J.; Lanzavecchia, A. Inflammatory stimuli induce accumulation of MHC class II complexes on dendritic cells. Nature 1997, 388, 782-787.
14. Pierre, P.; Turley, S.J.; Gatti, E., Hull, M.; Meltzer, J.; Mirza, A.; Inaba, K.; Steinman, R.M.; Mellman, I. Developmental regulation of MHC class II transport in mouse dendritic cells. Nature 1997, 388, 787-792.
15. Shin, J.S.; Ebersold, M.; Pypaert, M.; Delamarre, L.; Hartley, A.; Mellman, I. Surface expression of MHC class II in dendritic cells is controlled by regulated ubiquitination. Nature 2006, 444, 115-118.
16. Turley, S.J.; Inaba, K.; Garrett, W.S.; Ebersold, M.; Unternaehrer, J.; Steinman, R.M.; Mellman, I. Transport of peptide-MHC class II complexes in developing dendritic cells. Science 2000, 288, 522-527.
17. Wilson, N.S.; El-Sukkari, D.; Villadangos, J.A. Dendritic cells constitutively present self antigens in their immature state in vivo and regulate antigen presentation by controlling the rates of MHC class II synthesis and endocytosis. Blood 2004, 103, 2187-2195.
18. Inaba, K.; Witmer-Pack, M.; Inaba, M.; Hathcock, K.S.; Sakuta, H.; Azuma, M., Yagita, H.; Okumura, K.; Linsley, P.S.; Ikehara, S.; Muramatsu, S.; Hodes, R.J.; Steinman, R.M. The tissue distribution of the B7-2 costimulator in mice: abundant expression on dendritic cells in situ and during maturation in vitro. J. Exp. Med. 1994, 180, 1849-1860.
19. Larsen, C.P.; Ritchie, S.C.; Pearson, T.C.; Linsley, P.S.; Lowry, R.P. Functional expression of the costimulatory molecule, B7/BB1, on murine dendritic cell populations. J. Exp. Med. 1992, 176, 1215-1220.
20. Reise S C.; Hieny, S.; Scharton-Kersten, T.; Jankovic, D.; Charest, H.; Germain, R.N.; Sher, A. In vivo microbial stimulation induces rapid CD40 ligand-independent production of interleukin 12 by dendritic cells and their redistribution to T cell areas. J. Exp. Med. 1997, 186, 1819-1829.
21. Whelan, M.; Harnett, M.M.; Houston, K.M.; Patel, V.; Harnett, W.; Rigley, K.P. A filarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J. Immunol. 2000, 164, 6453-6460.
22. Kapsenberg, M.L. Dendritic-cell control of pathogen-driven T-cell polarization. Nat. Rev. Immunol. 2003, 3, 984-993.
23. Hackstein, H.; Thomson, A.W. Dendritic cells: Emerging pharmacological targets of immunosuppressive drugs. Nat. Rev. Immunol. 2004, 4, 24-34.
24. Wacnik, P.W.; Luhr, K.M.; Hill, R.H.; Ljunggren, H.G.; Kristensson, K.; Svensson, M. Cannabinoids affect dendritic cell (DC) potassium channel function and modulate DC T cell stimulatory capacity. J. Immunol. 2008, 181, 3057-3066.
25. Matias, I.; Pochard, P.; Orlando, P.; Salzet, M.; Pestel, J.; Di Marzo, V. Presence and regulation of the endocannabinoid system in human dendritic cells. Eur. J. Biochem. 2002, 269, 3771-3778.
26. Pandey, R.; Mousawy, K.; Nagarkatti, M.; Nagarkatti, P. Endocannabinoids and immune regulation. Pharmacol. Res. 2009, 60, 85-92.
27. Lu, T., Newton, C.; Perkins, I.; Friedman, H.; Klein, T.W. Cannabinoid treatment suppresses the T-helper cell-polarizing function of mouse dendritic cells stimulated with Legionella pneumophila infection. J. Pharmacol.Exp. Ther. 2006, 319, 269-276.
28. Noverr, M.C.; Erb-Downward, J.R.; Huffnagle, G.B. Production of eicosanoids and other oxylipins by pathogenic eukaryotic microbes. Clin. Microbiol. Rev. 2003, 16, 517-533.
29. Di Marzo, V.; Bisogno, T.; De Petrocellis, L.; Melck, D.; Orlando, P.; Wagner, J.A.; Kunos, G. Biosynthesis and inactivation of the endocannabinoid 2-arachidonoylglycerol in circulating and tumoral macrophages. Eur. J. Biochem. 1999, 264, 258-267.
30. Maccarrone, M.; Bari, M.; Battista, N.; Finazzi-Agro, A. Endocannabinoid degradation, endotoxic shock and inflammation. Curr. Drug Targets Inflamm. Allergy 2002, 1, 53-63.
31. Liu, J., Li, H.; Burstein, S.H.; Zurier, R.B.; Chen, J.D. Activation and binding of peroxisome proliferator-activated receptor gamma by synthetic cannabinoid ajulemic acid. Mol. Pharmacol. 2003, 63, 983-992.
32. Berdyshev, E.V. Cannabinoid receptors and the regulation of immune response. Chem. Phys. Lipids 2000, 108, 169-190.
33. Klein, T.W.; Lane, B., Newton, C.A.; Friedman, H. The cannabinoid system and cytokine network. Proc. Soc. Exp. Biol. Med. 2000, 225, 1-8.
34. Smith, S.R.; Terminelli, C.; Denhardt, G. Effects of cannabinoid receptor agonist and antagonist ligands on production of inflammatory cytokines and anti-inflammatory interleukin-10 in endotoxemic mice. J. Pharmacol. Exp. Ther. 2000, 293, 136-150.
35. Di Filippo, C.; Rossi, F.; Rossi, S.; D'Amico, M. Cannabinoid CB2 receptor activation reduces mouse myocardial ischemia-reperfusion injury: Involvement of cytokine/chemokines and PMN. J. Leukoc. Biol. 2004, 75, 453-459.
36. Klein, T.W.; Newton, C.A.; Nakachi, N.; Friedman, H. Delta 9-tetrahydrocannabinol treatment suppresses immunity and early IFN-gamma, IL-12, and IL-12 receptor beta 2 responses to Legionella pneumophila infection. J. Immunol. 2000, 164, 6461-6466.
37. Zhu, L.X.; Sharma, S.; Stolina, M.; Gardner, B.; Roth, M.D.; Tashkin, D.P.; Dubinett, S.M. Delta-9-tetrahydrocannabinol inhibits antitumor immunity by a CB2 receptor-mediated, cytokinedependent pathway. J. Immunol. 2000, 165, 373-380.
38. Derocq, J.M.; Jbilo, O.; Bouaboula, M.; Segui, M.; Clere, C.; Casellas, P. Genomic and functional changes induced by the activation of the peripheral cannabinoid receptor CB2 in the promyelocytic cells HL-60. Possible involvement of the CB2 receptor in cell differentiation. J. Biol. Chem. 2000, 275, 15621-15628.
39. Kishimoto, S.; Kobayashi, Y.; Oka, S., Gokoh, M.; Waku, K.; Sugiura, T. 2- Arachidonoylglycerol, an endogenous cannabinoid receptor ligand, induces accelerated production of chemokines in HL-60 cells. J. Biochem. 2004, 135, 517-524.
40. Eljaschewitsch, E.; Witting, A.; Mawrin, C.; Lee, T.; Schmidt, P.M.; Wolf, S.; Hoertnagl, H.; Raine, C.S.; Schneider-Stock, R.; Nitsch, R.; Ullrich, O. The endocannabinoid anandamide protects neurons during CNS inflammation by induction of MKP-1 in microglial cells. Neuron 2006, 49, 67-79.
41. Lambrecht, B.N, Immunologists getting nervous: Neuropeptides, dendritic cells and T cell activation. Respir. Res. 2001, 2, 133-138.
42. Luger, T.A. Neuromediators--a crucial component of the skin immune system. J. Dermatol. Sci. 2002, 30, 87-93.
43. Downing, J.E.; Miyan, J.A. Neural immunoregulation: Emerging roles for nerves in immune homeostasis and disease. Immunol. Today 2000, 21, 281-289.
44. Tournier, J.N.; Hellmann, A.Q. Neuro-immune connections: Evidence for a neuro-immunological synapse. Trends Immunol. 2003, 24, 114-115.
45. Langerhans, P. Über die nerven der menschlichen haut. Virchows Arch. Pathol. Anat. Physiol. 1868, 44, 325-337.
46. Egan, C.L.; Viglione-Schneck, M.J.; Walsh, L.J.; Green, B.; Trojanowski, J.Q.; Whitaker-Menezes, D. and Murphy, G.F. Characterization of unmyelinated axons uniting epidermal and dermal immune cells in primate and murine skin. J. Cutan. Pathol. 1998, 25, 20-29.
47. Gaudillere, A.; Misery, L.; Souchier, C.; Claudy, A.; Schmitt, D. Intimate associations between PGP9.5-positive nerve fibres and Langerhans cells. Br. J. Dermatol. 1996, 135, 343-344.
48. Hosoi, J.; Murphy, G.F.; Egan, C.L.; Lerner, E.A.; Grabbe, S.; Asahina, A.; Granstein, R.D. Regulation of Langerhans cell function by nerves containing calcitonin gene-related peptide. Nature 1993, 363, 159-163.
49. Muller, T. Intraepidermal free nerve fiber endings in the hairless skin of the rat as revealed by the zinc iodide-osmium tetroxide technique. Histol. Histopathol. 2000, 15, 493-498.
50. Markus, A.M.; Kockerling, F.; Neuhuber, W.L. Close anatomical relationships between nerve fibers and MHC class II-expressing dendritic cells in the rat liver and extrahepatic bile duct. Histochem. Cell Biol. 1998, 109, 409-415.
51. Ahluwalia, J.; Yaqoob, M.; Urban, L.; Bevan, S.; Nagy, I. Activation of capsaicin-sensitive primary sensory neurones induces anandamide production and release. J. Neurochem. 2003, 84, 585-591.
52. Friedman, M.; Cepero, M.L.; Klein, T; Friedman, H. Suppressive effect of delta 9-tetrahydrocannabinol in vitro on phagocytosis by murine macrophages. Proc. Soc. Exp. Biol. Med. 1986, 182, 225-228.
53. Coffey, R.G.; Yamamoto, Y.; Snella, E.; Pross, S. Tetrahydrocannabinol inhibition of macrophage nitric oxide production. Biochem. Pharmacol. 1996, 52, 743-751.
54. McCoy, K.L.; Gainey, D.; Cabral, G.A. delta 9-Tetrahydrocannabinol modulates antigen processing by macrophages. J. Pharmacol. Exp. Ther. 1995, 273, 1216-1223.
55. Watzl, B.; Scuderi, P.; Watson, R.R. Influence of marijuana components (THC and CBD) on human mononuclear cell cytokine secretion in vitro. Adv. Exp. Med. Biol. 1991, 288, 63-70.
56. Nakano, Y.; Pross, S.H.; Friedman, H. Modulation of interleukin 2 activity by delta 9-tetrahydrocannabinol after stimulation with concanavalin A, phytohemagglutinin, or anti-CD3 antibody. Proc. Soc. Exp. Biol. Med. 1992, 201, 165-168.
57. Maestroni, G.J. The endogenous cannabinoid 2-arachidonoyl glycerol as in vivo chemoattractant for dendritic cells and adjuvant for Th1 response to a soluble protein. FASEB J. 2004, 18, 1914-1916.
58. Do, Y.; McKallip, R.J.; Nagarkatti, M.; Nagarkatti, P.S. Activation through cannabinoid receptors 1 and 2 on dendritic cells triggers NF-kappaB-dependent apoptosis: Novel role for endogenous and exogenous cannabinoids in immunoregulation. J. Immunol. 2004, 173, 2373-2382.
59. 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, 431-439.
60. Yuan, M.; Kiertscher, S.M.; Cheng, Q.; Zoumalan, R.L; Tashkin, D.P.; Roth, M.D. Delta 9-Tetrahydrocannabinol regulates Th1/Th2 cytokine balance in activated human T cells. J. Neuroimmunol. 2002, 133, 124-131.
61. Bouma, G.; Burns, S.; Thrasher, A.J. Impaired T-cell priming in vivo resulting from dysfunction of WASp-deficient dendritic cells. Blood 2007, 110, 4278-4284.
62. Ramer, R.; Hinz, B. Cyclooxygenase-2 and tissue inhibitor of matrix metalloproteinases-1 confer the antimigratory effect of cannabinoids on human trabecular meshwork cells. Biochem. Pharmacol. 2010, doi:10.1016/j.bcp.2010.05.10.
63. Fischer, H.G.; Eder, C. Voltage-gated K+ currents of mouse dendritic cells. FEBS Lett. 1995, 373, 127-130.
64. George Chandy, K.; Wulff, H.; Beeton, C.; Pennington, M.; Gutman, G.A.; Cahalan, M.D. K+ channels as targets for specific immunomodulation. Trends Pharmacol. Sci. 2004, 25, 280-289.
65. Panyi, G.; Gaspar, R.; Krasznai, Z.; ter Horst, J.J.; Ameloot, M.; Aszalos, A.; Steels, P.; Damjanovich, S. Immunosuppressors inhibit voltage-gated potassium channels in human peripheral blood lymphocytes. Biochem. Biophys. Res. Commun. 1996, 221, 254-258.
66. Cahalan, M.D.; Chandy, K.G. Ion channels in the immune system as targets for immunosuppression. Curr. Opin. Biotechnol. 1997, 8, 749-756.
67. Mullen, K.M.; Rozycka, M.; Rus, H.; Hu, L.; Cudrici, C.; Zafranskaia, E.; Pennington, M.W.; Johns, D.C.; Judge, S.I.; Calabresi, P.A. Potassium channels Kv1.3 and Kv1.5 are expressed on blood-derived dendritic cells in the central nervous system. Ann. Neurol. 2006, 60, 118-127.
68. Conforti, L.; Petrovic, M.; Mohammad, D.; Lee, S.; Ma, Q.; Barone, S.; Filipovich, A.H. Hypoxia regulates expression and activity of Kv1.3 channels in T lymphocytes: A possible role in T cell proliferation. J. Immunol. 2003, 170, 695-702.
69. Shah, K.; Tom Blake, J.; Huang, C.; Fischer, P.; Koo, G.C. Immunosuppressive effects of a Kv1.3 inhibitor. Cell Immunol. 2003, 221, 100-106.
70. Garcia-Arencibia, M.; Gonzalez, S.; de Lago, E.; Ramos, J.A.; Mechoulam, R.; Fernandez-Ruiz, J. Evaluation of the neuroprotective effect of cannabinoids in a rat model of Parkinson's disease: importance of antioxidant and cannabinoid receptor-independent properties. Brain Res. 2007, 1134, 162-170.
71. Guzman, M. Cannabinoids: Potential anticancer agents. Nat. Rev. Cancer 2003, 3, 745-755.
72. Centonze, D.; Finazzi-Agro, A.; Bernardi, G.; Maccarrone, M. The endocannabinoid system in targeting inflammatory neurodegenerative diseases. Trends Pharmacol. Sci. 2007, 28, 180-187.
73. Baker, D.; Pryce, G, The therapeutic potential of cannabis in multiple sclerosis. Expert Opin. Investig. Drugs 2003, 12, 561-567.
74. Di Marzo, V.; Bifulco, M.; De Petrocellis, L. The endocannabinoid system and its therapeutic exploitation. Nat. Rev. Drug Discov. 2004, 3, 771-784.
75. Kunos, G.; Pacher, P. Cannabinoids cool the intestine. Nat. Med. 2004, 10, 678-679.
76. Mechoulam, R., Panikashvili, D. and Shohami, E. Cannabinoids and brain injury: Therapeutic implications. Trends Mol. Med. 2002, 8, 58-61.
77. Baldwin, G.C.; Tashkin, D.P.; Buckley, D.M.; Park, A.N.; Dubinett, S.M.; Roth, M.D. Marijuana and cocaine impair alveolar macrophage function and cytokine production. Am. J. Respir. Crit. Care Med. 1997, 156, 1606-1613.
78. Preet, A.; Ganju, R.K.; Groopman, J.E. Delta9-Tetrahydrocannabinol inhibits epithelial growth factor-induced lung cancer cell migration in vitro as well as its growth and metastasis in vivo. Oncogene 2008, 27, 339-346.
79. Galve-Roperh, I.; Sanchez, C.; Cortes, M.L.; Gomez del Pulgar, T.; Izquierdo, M.; Guzman, M. Anti-tumoral action of cannabinoids: Involvement of sustained ceramide accumulation and extracellular signal-regulated kinase activation. Nat. Med. 2000, 6, 313-319.
80. McAllister, S.D.; Christian, R.T.; Horowitz, M.P.; Garcia, A.; Desprez, P.Y. Cannabidiol as a novel inhibitor of Id-1 gene expression in aggressive breast cancer cells. Mol. Cancer Ther. 2007, 6, 2921-2927.
81. Carracedo, A.; Gironella, M.; Lorente, M.; Garcia, S.; Guzman, M.; Velasco, G.; Iovanna, J.L. Cannabinoids induce apoptosis of pancreatic tumor cells via endoplasmic reticulum stress-related genes. Cancer Res. 2006, 66, 6748-6755.
82. Blazquez, C.; Carracedo, A.; Barrado, L.; Real, P.J.; Fernandez-Luna, J.L.; Velasco, G.; Malumbres, M.; Guzman, M. Cannabinoid receptors as novel targets for the treatment of melanoma. FASEB J. 2006, 20, 2633-2635.
83. Weydt, P.; Hong, S.; Witting, A.; Moller, T.; Stella, N.; Kliot, M. Cannabinol delays symptom onset in SOD1 (G93A) transgenic mice without affecting survival. Amyotroph. Lateral Scler. 2005, 6, 182-184.
84. Sarfaraz, S.; Afaq, F.; Adhami, V.M.; Malik, A.; Mukhtar, H. Cannabinoid receptor agonistinduced apoptosis of human prostate cancer cells LNCaP proceeds through sustained activation of ERK1/2 leading to G1 cell cycle arrest. J. Biol. Chem. 2006, 281, 39480-39491.
85. Massa, F.; Marsicano, G.; Hermann, H.; Cannich, A.; Monory, K.; Cravatt, B.F.; Ferri, G.L.; Sibaev, A.; Storr, M.; Lutz, B. The endogenous cannabinoid system protects against colonic inflammation. J. Clin. Invest. 2004, 113, 1202-1209.
86. Kogan, N.M.; Schlesinger, M.; Priel, E., Rabinowitz, R.; Berenshtein, E.; Chevion, M.; Mechoulam, R. HU-331, a novel cannabinoid-based anticancer topoisomerase II inhibitor. Mol. Cancer Ther. 2007, 6, 173-183.
87. Qamri, Z.; Preet, A.; Nasser, M. W.; Bass, C.E.; Leone, G.; Barsky, S.H.; Ganju, R.K. Synthetic cannabinoid receptor agonists inhibit tumor growth and metastasis of breast cancer. Mol. Cancer Ther. 2009, 8, 3117-3129.
88. McKallip, R.J.; Lombard, C.; Fisher, M.; Martin, B.R.; Ryu, S.; Grant, S.; Nagarkatti, P.S.; Nagarkatti, M. Targeting CB2 cannabinoid receptors as a novel therapy to treat malignant lymphoblastic disease. Blood 2002, 100, 627-634.
89. Berdyshev, E.V.; Boichot, E.; Germain, N.; Allain, N.; Anger, J.P.; Lagente, V. Influence of fatty acid ethanolamides and delta9-tetrahydrocannabinol on cytokine and arachidonate release by mononuclear cells. Eur. J. Pharmacol. 1997, 330, 231-240.
90. McKallip, R.J.; Nagarkatti, M.; Nagarkatti, P.S. Delta-9-tetrahydrocannabinol enhances breast cancer growth and metastasis by suppression of the antitumor immune response. J. Immunol. 2005, 174, 3281-3289.
91. Mattes, J.; Hulett, M.; Xie, W.; Hogan, S.; Rothenberg, M.E.; Foster, P.; Parish, C. Immunotherapy of cytotoxic T cell-resistant tumors by T helper 2 cells: An eotaxin and STAT6-dependent process. J. Exp. Med. 2003, 197, 387-393.
92. Volpert, O.V.; Fong, T.; Koch, A.E.; Peterson, J.D.; Waltenbaugh, C.; Tepper, R.I.; Bouck, N.P. Inhibition of angiogenesis by interleukin 4. J. Exp. Med. 1998, 188, 1039-1046.
93. Matsuda, A.; Fukuda, S.; Matsumoto, K.; Saito, H. Th1/Th2 cytokines reciprocally regulate in vitro pulmonary angiogenesis via CXC chemokine synthesis. Am. J. Respir. Cell. Mol. Biol. 2008, 38, 168-175.
94. Sun, H.; Chung, W.C.; Ryu, S. H.; Ju, Z.; Tran, H. T.; Kim, E.; Kurie, J.M.; Koo, J.S. Cyclic AMP-responsive element binding protein- and nuclear factor-kappaB-regulated CXC chemokine gene expression in lung carcinogenesis. Cancer Prev. Res. (Phila Pa) 2008, 1, 316-328.
95. Lee, M.; Yang, K.H.; Kaminski, N.E. Effects of putative cannabinoid receptor ligands, anandamide and 2-arachidonyl-glycerol, on immune function in B6C3F1 mouse splenocytes. J. Pharmacol. Exp. Ther. 1995, 275, 529-536.
96. Di Marzo, V.; Melck, D.; Orlando, P.; Bisogno, T.; Zagoory, O.; Bifulco, M.; Vogel, Z.; De Petrocellis, L. Palmitoylethanolamide inhibits the expression of fatty acid amide hydrolase and enhances the anti-proliferative effect of anandamide in human breast cancer cells. Biochem. J. 2001, 358, 249-255.