The THC-induced suppression of Th1 polarization in response to Legionella pneumophila infection is not mediated by increases in corticosterone and PGE2

Journal of Leukocyte Biology

Volumn 76, Issue 4, 2004, Pages 854-861

  Newton, Catherine A ^a   Lu, Tangying ^a   Nazian, Stanley J ^a   Perkins, Izabella ^a   Friedman, Herman ^a   Klein, Thomas W ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Cannabinoids; IL 12; Prostaglandins; Th2 cells

Indexed keywords

2 (1 OCTYNYL)ADENOSINE; 5 (4 CHLORO 3 METHYLPHENYL) 1 (4 METHYLBENZYL) N (1,3,3 TRIMETHYLBICYCLO[2.2.1]HEPTAN 2 YL) 3 PYRAZOLECARBOXAMIDE; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR ANTAGONIST; CORTICOSTERONE; DRONABINOL; GAMMA INTERFERON; GLUCOCORTICOID; INDOMETACIN; INTERLEUKIN 12; MIFEPRISTONE; PROSTAGLANDIN E2; PROSTAGLANDIN SYNTHASE INHIBITOR; RIMONABANT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOSTERONE RELEASE; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME INHIBITION; FEMALE; IMMUNOMODULATION; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; METABOLITE; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROSTAGLANDIN RELEASE; TH1 CELL;

ANIMALS; BORNANES; CORTICOSTERONE; DINOPROSTONE; FEMALE; HORMONE ANTAGONISTS; IMMUNOSUPPRESSION; INTERFERON TYPE II; INTERLEUKIN-12; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MICE; MICE, INBRED BALB C; MIFEPRISTONE; PIPERIDINES; PYRAZOLES; RADIOIMMUNOASSAY; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; TETRAHYDROCANNABINOL; TH1 CELLS;

ANIMALIA; CANNABIS SATIVA; LEGIONELLA; LEGIONELLA PNEUMOPHILA;

EID: 4744342396     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0304184     Document Type: Article

References (56)

1. Klein, T., Newton, C., Friedman, H. (1998) Cannabinoid receptors and immunity. Immunol. Today 19, 373-381.
2. Klein, T. W., Lane, B., Newton, C. A., Friedman, H. (2000) The cannabinoid system and cytokine network. Proc. Soc. Exp. Biol. Med. 225, 1-8.
3. Klein, T. W., Newton, C., Larsen, K., Lu, L., Perkins, I., Nong, L., Friedman, H. (2003) The cannabinoid system and immune modulation. J. Leukoc. Biol. 74, 486-496.
4. Pertwee, R. G. (1997) Pharmacology of cannabinoid CB1 and CB2 receptors. Pharmacol. Ther. 74, 129-180.
5. Ledent, C., Valverde, O., Cossu, G., Petitet, F., Aubert, J. F., Beslot, F., Bohme, G. A., Imperato, A., Pedrazzini, T., Roques, B. P., Vassart, G., Fratta, W., Pannentier, M. (1999) Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 283, 401-404.
6. Zimmer, A., Zimmer, A. M., Hohmann, A. G., Herkenham, M., Bonner, T. I. (1999) Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc. Natl. Acad. Sci. USA 96, 5780-5785.
7. Buckley, N. E., McCoy, K. L., Mezey, E., Bonner, T., Zimmer, A., Felder, C. C., Glass, M. (2000) Immunomodulation by cannabinoids is absent in mice deficient for the cannabinoid CB(2) receptor. Eur. J. Pharmacol. 396, 141-149.
8. Newton, C. A., Klein, T. W., Friedman, H. (1994) Secondary immunity to Legionella pneumophila and Th1 activity are suppressed by δ-9- tetrahydrocannabinol injection. Infect. Immun. 62, 4015-4020.
9. 9-Tetrahydrocannabinol treatment suppresses immunity and early IFN-γ, IL-12, and IL-12 receptor β2 responses to Legionella pneumophila infection. J. Immunol. 164, 6461-6466.
10. Szabo, S. J., Dighe, A. S., Gubler, U., Murphy, K. M. (1997) Regulation of the interleukin (IL)-12R B2 subunit expression in developing T helper 1 (Th1) and Th2 cells. J. Exp. Med. 185, 817-824.
11. Pulendran, B., Palucka, K., Banchereau, J. (2001) Sensing pathogens and tuning immune responses. Science 293, 253-256.
12. Wu, C., Wang, X., Gadina, M., O'Shea, J. J., Presky, D. H., Magram, J. (2000) IL-12 receptor β 2 (IL-12R β 2)-deficient mice are defective in IL-12-mediated signaling despite the presence of high affinity IL-12 binding sites. J. Immunol. 165, 6221-6228.
13. Scott, P., Eaton, A., Gause, W. C., di Zhou, X., Hondowicz, B. (1996) Early IL-4 production does not predict susceptibility to Leishmania major. Exp. Parasitol. 84, 178-187.
14. Ramirez-Pineda, J. R., Frohlich, A., Berberich, C., Moll, H. (2004) Dendritic cells (DC) activated by CpG DNA ex vivo are potent inducers of host resistance to an intracellular pathogen that is independent of IL-12 derived from the immunizing DC. J. Immunol. 172, 6281-6289.
15. Pacifici, R., Zuccaro, P., Pichini, S., Roset, P. N., Poudevida, S., Farre, M., Segura, J., De la Torre, R. (2003) Modulation of the immune system in cannabis users. JAMA 289, 1929-1931.
16. Yuan, M., Kiertscher, S. M., Cheng, Q., Zoumalan, R., Tashkin, D. P., Roth, M. D. (2002) D9-tetrahydrocannabinol regulates Th1/Th2 cytokine balance in activated human T cells. J. Neuroimmunol. 133, 124-131.
17. Smith, S. R., Terminelli, C., Denhardt, G. (2001) Modulation of cytokine responses in Corynebacterium parvum-primed endotoxemic mice by centrally administered cannabinoid ligands. Eur. J. Pharmacol. 425, 73-83.
18. Zhu, L. X., Sharma, S., Stolina, M., Gardner, B., Roth, M. D., Tashkin, D. P., Dubinett, S. M. (2000) Δ-9-Tetrahydrocannabinol inhibits antitumor immunity by a CB2 receptor-mediated, cytokine-dependent pathway. J. Immunol. 165, 373-380.
19. Massi, P., Fuzio, D., Vigano, D., Sacerdote, P., Parolaro, D. (2000) Relative involvement of cannabinoid CB(1) and CB(2) receptors in the δ(9)-tetrahydrocannabinol-induced inhibition of natural killer activity. Eur. J. Pharmacol. 387, 343-347.
20. Kuo, C., Leiden, J. (1999) Transcriptional regulation of T lymphocyte development and function. Annu. Rev. Immunol. 17, 149-187.
21. Moser, M., Murphy, K. (2000) Dendritic cell regulation of Th1-Th2 development. Nat. Immunol. 1, 199-205.
22. Das, J., Chen, C-H., Yang, L., Cohn, L, Ray, P., Ray, A. (2001) A critical role for NF-κB in GATA3 expression and Th2 differentiation in allergic airway inflammation. Nat. Immunol. 2, 45-50.
23. He, J., Gurunathan, S., Iwasaki, A., Ash-Shaheed, B., Kelsall, B. (2000) Primary role for Gi protein signaling in the regulation of interleukin 12 production and the induction of T helper cell type 1 responses. J. Exp. Med. 191, 1605-1610.
24. Wu, C-Y., Wang, K., McDyer, J. F., Seder, R. A. (1998) Prostaglandin E2 and dexamethasone inhibit IL-12 receptor expression and IL-12 responsiveness. J. Immunol. 161, 2723-2730.
25. Harris, S. G., Padilla, J., Koumas, L., Ray, D., Phipps, R. P. (2002) Prostaglandins as modulators of immunity. Trends Immunol. 23, 144-150.
26. Visser, J., van Boxel-Dezaire, A., Methorst, D., Brunt, T., de Kloet, E. R., Nagelkerken, L. (1998) Differential regulation of interleukin-10 (IL-10) and IL-12 by glucocorticoids in vitro. Blood 91, 4255-4264.
27. Miyaura, H., Iwata, M. (2002) Direct and indirect inhibition of Th1 development by progesterone and glucocorticoids. J. Immunol. 168, 1087-1094.
28. Newton, C., McHugh, S., Widen, R., Nakachi, N., Klein, T., Friedman, H. (2000) Induction of interleukin-4 (1L-4) by Legionella pneumophila infection in BALB/c mice and regulation of tumor necrosis factor α, 1L-6, and IL-1β. Infect. Immun. 68, 5234-5240.
29. Flesch, I. E., Wandersee, A., Kaufmann, S. H. (1997) IL-4 secretion by CD4+ NKI+ T cells induces monocyte chemoattractant protein-1 in early listeriosis. J. Immunol. 159, 7-10.
30. Hunter, S. A., Audette, C. A., Burstein, S. (1991) Elevation of brain prostaglandin E2 levels in rodents by δ 1-tetrahydrocannabinol. Prostaglandins Leukot. Essent. Fatty Acids 43, 185-190.
31. Weidenfeld, J., Feldman, S., Mechoulam, R. (1994) Effect of brain constituent anandamide, a cannabinoid receptor agonist, on the hypothalamo-pituitary-adrenal axis in the rat. Neuroendocrinology 59, 110-112.
32. 1-tetrahydrocannabinol, in intact and in hypothalamic deafferentated male rats. Exp. Brain Res. 46, 85-88.
33. Marsicano, G., Lutz, B. (1999) Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur. J. Neurosci. 11, 4213-4225.
34. Wenger, T., Ledent, C., Csernus, V., Gerendai, I. (2001) The central cannabinoid receptor inactivation suppresses endocrine reproductive functions. Biochem. Biophys. Res. Commun. 284, 363-368.
35. Chiappelli, F., Manfrini, E., Franceschi, C., Cossarizza, A., Black, K. L. (1994) Steroid regulation of cytokines. Relevance for TH1-to-TH2 shift? Ann. N. Y. Acad. Sci. 746, 204-215.
36. Kalinski, P., Schuitemaker, J. H., Hilkens, C. M., Kapsenberg, M. L. (1998) Prostaglandin E2 induces the final maturation of IL-12-deficient CD1a+CD83+ dendritic cells: the levels of IL-12 are determined during the final dendritic cell maturation and are resistant to further modulation. J. Immunol. 161, 2804-2809.
37. Cadepond, F., Ulmann, A., Baulieu, E. E. (1997) RU486 (mifepristone): mechanisms of action and clinical uses. Annu. Rev. Med. 48, 129-156.
38. Valiveti, S., Hammell, D. C., Earles, D. C., Stinchcomb, A. L. (2004) In vitro/in vivo correlation studies for transdermal δ8-THC development. J. Pharm. Sci. 93, 1154-1164.
39. Naef, M., Russmann, S., Petersen-Felix, S., Brenneisen, R. (2004) Development and pharmacokinetic characterization of pulmonal and intravenous δ-9-tetrahydrocannabinol (THC) in humans. J. Pharm. Sci. 93, 1176-1184.
40. Zhang, D., Kishihara, K., Wang, B., Mizobe, K., Kubo, C., Nomoto, K. (1998) Restraint stress-induced immunosuppression by inhibiting leukocyte migration and Th1 cytokine expression during the intraperitoneal infection of Listeria monocytogenes. J. Neuroimmunol. 92, 139-151.
41. Flint, M. S., Tinkle, S. S. (2001) C57BL/6 mice are resistant to acute restraint modulation of cutaneous hypersensitivity. Toxicol. Sci. 62, 250-256.
42. Manzanares, J., Corchero, J., Fuentes, J. A. (1999) Opinid and cannabinoid receptor-mediated regulation of the increase in adrenocorticotropin hormone and corticosterone plasma concentrations induced by central administration of δ(9)-tetrahydrocannabinol in rats. Brain Res. 839, 173-179.
43. Franchimont, D., Galon, J., Gadina, M., Visconti, R., Zhou, Y., Aringer, M., Frucht, D. M., Chrousos, G. P., O'Shea, J. J. (2000) Inhibition of Th1 immune response by glucocorticoids: dexamethasone selectively inhibits IL-12-induced Stat4 phosphorylation in T lymphocytes. J. Immunol. 164, 1768-1774.
44. Mansilla-Rosello, A., Ferron-Orihuela, J. A., Ruiz-Cabello, F., Carrote-Lara, D., Fernandez-Mondejar, E., Delgado-Carraseo, M. L. (1997) Differential effects of IL-1 β and ibuprofen after endotoxic challenge in mice. J. Surg. Res. 67, 199-204.
45. Wenger, T., Moldrich, G. (2002) The role of endocannabinoids in the hypothalamic regulation of visceral function. Prostaglandins Leukot. Essent. Fatty Acids 66, 301-307.
46. Wenger, T., Fernandez-Ruiz, J. J., Hamos, J. A. (1999) Immunocytochemical demonstration of CB1 cannabinoid receptors in the anterior lobe of the pituitary gland. J. Neuroendocrinol. 11, 873-878.
47. Welch, S. P., Huffman, J. W., Lowe, J. (1998) Differential blockade of the antinociceptive effects of centrally administered cannabinoids by SRI41716A. J. Pharmacol. Exp. Ther. 286, 1301-1308.
48. Maccarrone, M., Bari, M., Battista, N., Finazzi-Agro, A. (2002) Endocannabinoid degradation, endotoxic shock and inflammation. Curr. Drug Targets Inflamm. Allergy 1, 53-63.
49. Mirani, M., Elenkov, I., Volpi, S., Hiroi, N., Chrousos, G. P., Kino, T. (2002) HIV-1 protein Vpr supresses IL-12 production from human monocytes by enhancing glucocorticoid action: potential implications of Vpr coactivator activity for the innate and cellular immunity deficits observed in HIV-1 infection. J. Immunol. 169, 6361-6568.
50. Alesci, S., De Martino, M. U., Mirani, M., Benvenga, S., Trimarchi, F., Kino, T., Chrousos, G. P. (2003) L-carnitine: a nutritional modulator of glucocorticoid receptor functions. FASEB J. 17, 1553-1555.
51. 2 inhibits production of Th1 lymphokines but not of Th2 lymphokines. J. Immunol. 146, 108-113.
52. Kalinski, P., Hilkens, C. M., Snijders, A., Snijdewint, F. G. Kapsenberg, M. L. (1997) IL-12-deficient dendritic cells, generated in the presence of prostaglandin E2, promote type 2 cytokine production in maturing human naive T helper cells. J. Immunol. 159, 28-35.
53. Kuroda, E., Sugiura, T., Zeki, K., Yoshida, Y., Yamashita, U. (2000) Sensitivity difference to the suppressive effect of prostaglandin E among mouse strains: a possible mechanism to polarize Th2 type response in BALB/c mice. J. Immunol. 164, 2386-2395.
54. Li, J., Padigel, U. M., Scott, P., Farell, J. P. (2002) Combined treatment with interleukin-12 and indomethacin promotes increased resistance in BALB/c mice with established Leishmania major infections. Infect. Immun. 70, 5715-5720.
55. Hunter, S. A., Burstein, S. H. (1997) Receptor mediation in cannabinoid-stimulated arachidonic acid mobilization and anandamide synthesis. Life Sci. 60, 1563-1573.
56. Klein, T. W., Newton, C., Larsen, K., Chou, J., Perkins, I., Lu, L., Nong, L., Friedman, H. (2004) Cannabinoid receptors and T helper biasing. J. Neuroimmunol. 147, 91-94.