Δ9-Tetrahydrocannabinol-induced anti-inflammatory responses in adolescent mice switch to proinflammatory in adulthood

Journal of Leukocyte Biology

Volumn 96, Issue 4, 2014, Pages 523-534

  Moretti, Sarah ^a   Castelli, Mara ^a   Franchi, Silvia ^a   Raggi, Maria Augusta ^b   Mercolini, Laura ^b   Protti, Michele ^b   Somaini, Lorenzo ^c   Panerai, Alberto E ^a   Sacerdote, Paola ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c Addiction Treatment Centre   (Italy)

Author keywords

Cytokines; Immune response; Liquid chromatography mass spectrometry; Marijuana

Indexed keywords

ANTIINFLAMMATORY AGENT; CYTOKINE; DRONABINOL; HEMOCYANIN; IMMUNOGLOBULIN M; KEYHOLE-LIMPET HEMOCYANIN;

ANIMAL; BIOSYNTHESIS; CYTOLOGY; DRUG EFFECTS; IMMUNOLOGY; MACROPHAGE; MALE; METABOLISM; MOUSE; PHAGOCYTOSIS; SPLEEN;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CYTOKINES; DRONABINOL; HEMOCYANIN; IMMUNOGLOBULIN M; MACROPHAGES; MALE; MICE; PHAGOCYTOSIS; SPLEEN;

EID: 84907528702     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3HI0713-406RR     Document Type: Article

References (71)

1. Klein, T. W. (2005) Cannabinoid-based drugs as anti-inflammatory therapeutics. Nat. Rev. Immunol. 5, 400-411.
2. Mackie, K. (2006) Cannabinoid receptors as therapeutic targets. Annu. Rev. Pharmacol. Toxicol. 46, 101-122.
3. Pertwee, R. G. (2009) Emerging strategies for exploiting cannabinoid receptor agonists as medicines. Br. J. Pharmacol. 156, 397-411.
4. Pertwee, R. G., Ross, R. A. (2002) Cannabinoid receptors and their ligands. Prostaglandins Leukot. Essent. Fatty Acids 66, 101-121.
5. Massi, P., Vaccani, A., Parolaro, D. (2006) Cannabinoids, immune system and cytokine network. Curr. Pharm. Des. 12, 3135-3146.
6. Berdyshev, E. V. (2000) Cannabinoid receptors and the regulation of immune response. Chem. Phys. Lipids 108, 169-190.
7. Elsohly, M., Slade, D. (2005) Chemical constituents of marijuana: the complex mixture of natural cannabinoids. Life Sci. 78, 539-548.
8. Sacerdote, P., Massi, P., Panerai, A. E., Parolaro, D. (2000) In vivo and in vitro treatment with the synthetic cannabinoid CP55, 940 decreases the in vitro migration of macrophages in the rat: involvement of both CB1 and CB2 receptors. J. Neuroimmunol. 109, 155-163.
9. Massi, P., Fuzio, D., Viganò, 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.
10. Cabral, G. A., Dove Pettit, D. A. (1998) Drugs and immunity: cannabinoids and their role in decreased resistance to infectious disease. J. Neuroimmunol. 83, 116-123.
11. 9Tetrahydrocannabinol treatment suppresses immunity and early IFN-γ, IL-12, and IL-12 receptor 2 responses to Legionella pneumophila infection. J. Immunol. 164, 6461-6466.
12. Klein, T. W., Cabral, G. A. (2006) Cannabinoid- induced immune suppression and modulation of antigen-presenting cells. J. Neuroimmune Pharmacol. 1, 50-64.
13. Pandey, R., Hegde, V. L., Nagarkatti, M., Nagarkatti, P. S. (2011) Targeting cannabinoid receptors as a novel approach in the treatment of graftversus- host disease: evidence from an experimental murine model. J. Pharmacol. Exp. Ther. 338, 819-828.
14. Nagarkatti, P., Pandey, R., Rieder, S. A., Hegde, V. L., Nagarkatti, M. (2009) Cannabinoids as novel anti-inflammatory drugs. Future Med. Chem. 1, 1333-1349.
15. Newton, C. A., Chou, P. J., Perkins, I., Klein, T. W. (2009) CB(1) and CB(2) cannabinoid receptors mediate different aspects of Δ-9-tetrahydrocannabinol (THC)-induced T helper cell shift following immune activation by Legionella pneumophila infection. J. Neuroimmune Pharmacol. 4, 92-102.
16. Cabral, G. A. (2006) Drugs of abuse, immune modulation and AIDS. J. Neuroimmune Pharmacol. 1, 280-295.
17. Friedman, H., Newton, C., Klein, T. W. (2003) Microbial infections, immunomodulation, and drugs of abuse. Clin. Microbiol. Rev. 16, 209-219.
18. Kaushik, K.S., Kapila, K., Praharaj, A. K. (2011) Shooting up: the interface of microbial infections and drug abuse. J. Med. Microbiol. 60, 408-422.
19. Center for Substance Abuse Treatment (2004) “Substance abuse treatment and familiy therapy”. Treatment Improvement Protocol (TIP) Series, No. 39, DHHS Publication No. (SMA) 04-3957. Substance Abuse and Mental Health Services Administration, Rockville, MD, USA, from http:// www.ncbi.nlm.nih.gov/books/NBK64265/.
20. Rubino, T., Viganò, D., Realini, N., Guidali, C., Braida, D., Capurro, V., Castiglioni, C., Cherubino, F., Romualdi, P., Candeletti, S., Sala, M., Parolaro, D. (2008) Chronic Δ 9-tetrahydrocannabinol during adolescence provokes sex-dependent changes in the emotional profile in adult rats: behavioral and biochemical correlates. Neuropsychopharmacology 33, 2760-2771.
21. Rubino, T., Zamberletti, E., Parolaro, D. (2012) Adolescent exposure to cannabis as a risk factor for psychiatric disorders. J. Psychopharmacol. 26, 177-188.
22. Tomasiewicz, H. C., Jacobs, M. M., Wilkinson, M. B., Wilson, S. P., Nestler, E. J., Hurd, Y. L. (2012) Proenkephalin mediates the enduring effects of adolescent cannabis exposure associated with adult opiate vulnerability. Biol. Psychiatry 72, 803-810.
23. Gonzalez, R., Swanson, J. M. (2012) Long-term effects of adolescent-onset and persistent use of cannabis. Proc. Natl. Acad. Sci. USA 109, 15970.
24. Blakemore, S. J. (2013) Teenage kicks: cannabis and the adolescent brain. Lancet 381, 888-889.
25. Batalla, A., Bhattacharyya, S., Yücel, M., Fusar-Poli, P., Crippa, J. A., Nogué, S., Torrens, M., Pujol, J., Farré, M., Martin-Santos, R. (2013) Structural and functional imaging studies in chronic cannabis users: a systematic review of adolescent and adult findings. PLoS One 8, e55821.
26. Massi, P., Sacerdote, P., Ponti, W., Fuzio, D., Manfredi, B., Viganò, D., Rubino, T., Bardotti, M., Parolaro, D. (1998) Immune function alterations in mice tolerant to Δ 9-tetrahydrocannabinol: functional and biochemical parameters. J. Neuroimmunol. 92, 60-66.
27. Lombard, C., Hegde, V. L., Nagarkatti, M., Nagarkatti, P. S. (2011) Perinatal exposure to Δ9-tetrahydrocannabinol triggers profound defects in T cell differentiation and function in fetal and postnatal stages of life, including decreased responsiveness to HIV antigens. J. Pharmacol. Ther. 339, 607-617.
28. Zamberletti, E.,Beggiato, S., Steardo Jr., L., Prini, P., Antonelli, T., Ferraro, L., Rubino, T., Parolaro, D. (2014) Alteration of prefrontal cortex GABAergic transmission in the complex psychotic-like phenotype induced by adolescent Δ-9-tetrahydrocannabinol exposure in rats. Neurobiol. Dis. 63, 35-47.
29. Martucci, C., Franchi, S., Lattuada, D., Panerai, A. E., Sacerdote, P. (2007) Differential involvement of RelB in morphine-induced modulation of chemotaxis, NO, and cytokine production in murine macrophages and lymphocytes. J. Leukoc. Biol. 81, 344-354.
30. Martucci, C., Trovato, A. E., Costa, B., Borsani, E., Franchi, S., Magnaghi, V., Panerai, A. E., Rodella, L. F., Valsecchi, A. E., Sacerdote, P., Colleoni, M. (2008) The purinergic antagonist PPADS reduces pain related behaviours and interleukin-1 β, interleukin-6, iNOS and nNOS overproduction in central and peripheral nervous system after peripheral neuropathy in mice. Pain 137, 81-95.
31. Sacerdote, P., Manfredi, B., Gaspani, L., Panerai, A. E. (2000) The opioid antagonist naloxone induces a shift from type 2 to type 1 cytokine pattern in BALB/cJ mice. Blood 95, 2031-2036.
32. Mercolini, L., Mandrioli, R., Sorella, V., Somaini, L., Giocondi, D., Serpelloni, G., Raggi, M. A. (2013) Dried blood spots: liquid chromatography- mass spectrometry analysis of Δ9-tetrahydrocannabinol and its main metabolites. J. Chromatogr. A 1271, 33-40.
33. Watanabe, K., Yamaori, S., Funahashi, T., Kimura, T., Yamamoto, I. (2007) Cytochrome P450 enzymes involved in the metabolism of tetrahydrocannabinols and cannabinol by human hepatic microsomes. Life Sci. 80, 1415-1419.
34. Hunault, C. C., Mensinga, T. T., de Vries, I., Kelholt-Dijkman, H. H., Hoek, J., Kruidenier, M., Leenders, M. E., Meulenbelt, J. (2008) Δ-9-Tetrahydrocannabinol (THC) serum concentrations and pharmacological effects in males after smoking a combination of tobacco and cannabis containing up to 69 mg THC. Psychopharmacology 201, 171-181.
35. Gustafson, R. A., Kim, I., Stout, P. R., Klette, K. L., George, M. P., Moolchan, E. T., Levine, B., Huestis, M. A. (2004) Urinary pharmacokinetics of 11-nor-9-carboxy-delta9-tetrahydrocannabinol after controlled oral Δ9-tetrahydrocannabinol administration. J. Anal. Toxicol. 28, 160-167.
36. McKallip, R. J., Lombard, C., Martin, B. R., Nagarkatti, M., Nagarkatti, P. S. (2002) Δ(9)-Tetrahydrocannabinol-induced apoptosis in the thymus and spleen as a mechanism of immunosuppression in vitro and in vivo. J. Pharmacol. Exp. Ther. 302, 451-465.
37. Pickles, A., Pickering, K., Simonoff, E., Silberg, J., Meyer, J., Maes, H. (1998) Genetic “clocks” and “soft” events: a twin model for pubertal development and other recalled sequences of developmental milestones, transitions, or ages at onset. Behav. Genet. 28, 243-253.
38. Spear, L. P., Brake, S. C. (1983) Periadolescence: age-dependent behaviour and psychopharmacological responsivity in rats. Develop. Psychobiol. 16, 83-109.
39. Spear, L. P. (2000) The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. Rev. 24, 417-463.
40. Odell, W. D. (1990) Sexual maturation in the rat. In Control of the Onset of Puberty (M. M. Grumbach, P. C. Sizonenko, M. L. Aubert, eds.), Williams &Wilkins, Baltimore, MD, USA, 183-210.
41. Ferrari, D., Pizzirani, C., Adinolfi, E., Lemoli, R. M., Curti, A., Idzko, M., Panther, E., Di Virgilio, F. (2007) The P2X7 receptor: a key player in IL-1 processing and release. J. Immunol. 179, 8569.
42. Zheng, Z. M., Specter, S. C. (1996) Δ-9-Tetrahydrocannabinol suppresses tumor necrosis factor α maturation and secretion but not its transcription in mouse macrophages. Int. J. Immunopharmacol. 18, 53-68.
43. Newton, C. A., Lu, T., Nazian, S. J., Perkins, I., Friedman, H., Klein, T. W. (2004) The THC-induced suppression of Th1 polarization in response to Legionella pneumophila infection is not mediated by increases in corticosterone and PGE2. J. Leukoc. Biol. 76, 854-861.
44. Underhill, D. M., Goodridege, H. S. (2012) Information processing during phagocytosis. Nat. Rev. Immunol. 12, 492-502.
45. Agudelo, M., Newton, C., Widen, R., Sherwood, T., Nong, L., Friedman, H., Klein, T. W. (2008) Cannabinoid receptor 2 (CB2) mediates immunoglobulin class switching from IgM to IgE in cultures of murine-purified B lymphocytes. J. Neuroimmune Pharmacol. 3, 35-42.
46. Newton, C. A., Klein, T. W. (2012) Cannabinoid 2 (CB2) receptor involvement in the down-regulation but not up-regulation of serum IgE levels in immunized mice. J. Neuroimmune Pharmacol. 7, 591-598.
47. Ngaotepprutaram, T., Kaplan, B. L.,Carney, S., Crawford, R., Kaminski, N. E. (2013) Suppression of Δ-tetrahydrocannabinol of the primary immunoglobulin M response by human peripheral blood B cells is associated with impaired STAT3 activation. Toxicology 310C, 84-91.
48. Springs, A. E., Karmaus, P. W., Crawford, R. B., Kaplan, B. L., Kaminski, N. E. (2008) Effects of targeted deletion of cannabinoid receptors CB1 and CB2 on immune competence and sensitivity to immune modulation by Δ9-tetrahydrocannabinol. J. Leukoc. Biol. 84, 1574-1584.
49. Takeda, K., Tanaka, T., Shi, W., Matsumoto, M., Minami, M., Kashiwamura, S., Nakanishi, K., Yoshida, N., Kishimoto, T., Akira, S. (1996) Essential role of Stat6 in IL-4 signalling. Nature 380, 627-630.
50. Gascon, M., Morales, E., Sunyer, J., Vrijheid, M. (2013) Effects of persistent organic pollutants on the developing respiratory and immune systems: a systematic review. Environ. Int. 52, 51-65.
51. Jiang, S., Fu, Y., Williams, J., Wood, J., Pandarinathan, L., Avraham, S., Makriyannis, A., Avraham, S., Avraham, H.K. (2007) Expression and function of cannabinoid receptors CB1 and CB2 and their cognate cannabinoid ligands in murine embryonic stem cells. PLoS One 2, e641.
52. Lu, T., Newton, C., Perkins, I., Friedman, H., Klein, T. W. (2006) Cannabinoid treatment suppresses the T-helper cell-polarizing function of mouse dendritic cells stimulated with Legionella pneumophila infection. J. Pharmacol. Exp. Ther. 319, 269-276.
53. Hegde, V. L., Nagarkatti, M., Nagarkatti, P. S. (2010) Cannabinoid receptor activation leads to massive mobilization of myeloid-derived suppressor cells with potent immunosuppressive properties. Eur. J. Immunol. 40, 3358-3371.
54. Morris, C. V., Di Nieri, J. A., Szutorisz, H., Hurd, Y. L. (2011) Molecular mechanisms of maternal cannabis and cigarette use on human neurodevelopment. Eur. J. Neurosci. 34, 1574-1583.
55. Schwarz, J. M., Hutchinson, M. R., Bilbo, S. D. (2011) Early-life experience decreases drug-induced reinstatement of morphine CPP in adulthood via microglial-specific epigenetic programming of anti-inflammatory IL-10 expression. J. Neurosci. 31, 17835-17847.
56. McCormick, C. M., Mathews, I. (2007) HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressor. Pharmacol. Biochem. Behav. 86, 220-233.
57. 9-THC) attenuates mouse sperm motility and male fecundity. Br. J. Pharmacol. 165, 2575-2583.
58. Roche, M., Diamond, M., Kelly, J. P., Finn, D. P. (2006) In vivo modulation of LPS-induced alterations in brain and peripheral cytokines and HPA axis activity by cannabinoids. J. Neuroimmunol. 181, 57-67.
59. Steiner, M. A., Wotjak, C. T. (2008) Role of the endocannabinoid system in regulation of the hypothalamic-pituitary-adrenocortical axis. Prog. Brain Res. 170, 397-432.
60. Schramm-Sapyta, N. L., Cha, Y. M., Chaudhry, S., Wilson, W. A., Swartzwelder, H. S., Kuhn, C. M. (2007) Differential anxiogenic, aversive, and locomotor effects of THC in adolescent and adult rats. Psychopharmacology 191, 867-877.
61. Armario, A. (2010) Activation of the hypothalamic pituitary adrenal axis by addictive drugs: different pathways, common outcome. Trends Pharmacol. Sci. 31, 318-325.
62. Huizink, A. C., Ferdinand, R. F., Ormel, J., Verhulst, F. C. (2006) Hypothalamic- pituitary-adrenal axis activity and early onset of cannabis use. Addiction 101, 1581-1588.
63. van Leeuwen, A. P., Creemers, H. E., Greaves-Lord, K., Verhulst, F. C., Ormel, J., Huizink, A. C. (2011) Hypothalamic-pituitary-adrenal axis reactivity to social stress and adolescent cannabis use: the TRAILS study. Addiction 106, 1484-1492.
64. Miyaura, H., Iwata, M. (2002) Direct and indirect inhibition of Th1development by progesterone and glucocorticoids. J. Immunol. 168, 1087-1094.
65. 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.
66. 9-tetrahydrocannabinol and its metabolites in mouse brain following marijuana inhalation determined by high-performance liquid chromatography-tandem mass spectrometry. J. Anal. Toxicol. 34, 516-520.
67. Ryberg, E., Larsson, N., Sjögren, S., Hjorth, S., Hermansson, N. O., Leonova, J., Elebring, T., Nilsson, K., Drmota, T., Greasley, P. J. (2007) The orphan receptor GPR55 is a novel cannabinoid receptor. Br. J. Pharmacol. 152, 1092-1101.
68. Gupta, S., Grieco, M. H., Cushman Jr., P. (1974) Impairment of rosetteforming T lymphocytes in chronic marihuana smokers. N. Engl. J. Med. 291, 874-877.
69. Petersen, B. H., Lemberger, L., Graham, J., Dalton, B. (1975) Alterations in the cellular-mediated immune responsiveness of chronic marihuana smokers. Psychopharmacol. Commun. 1, 67-74.
70. Cohen, S. (1976) The 94-day cannabis study. Ann. N. Y. Acad. Sci. 282, 211-220.
71. Liu, Q. R., Pan, C. H., Hishimoto, A., Li, C. Y., Xi, Z. X., Llorente-Berzal, A., Viveros, M. P., Ishiguro, H., Arinami, T., Onaivi, E. S. Uhl, G. R. (2009) Species differences in cannabinoid receptor 2 (CNR2 gene): identification of novel human and rodent CB2 isoforms, differential tissue expression and regulation by cannabinoid receptor ligands. Genes Brain Behav. 8, 519-530.