Perinatal exposure to Δ 9-tetrahydrocannabinol triggers profound defects in T cell differentiation and function in fetal and postnatal stages of life, including decreased responsiveness to HIV antigens

Journal of Pharmacology and Experimental Therapeutics

Volumn 339, Issue 2, 2011, Pages 607-617

  Lombard, Catherine ^a   Hegde, Venkatesh L ^a   Nagarkatti, Mitzi ^a   Nagarkatti, Prakash S ^a  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 IODO 3 (4 METHOXYBENZOYL) 2 METHYL 1 (2 MORPHOLINOETHYL)INDOLE; CANNABINOID RECEPTOR; CASPASE; GAG PROTEIN; GLYCOPROTEIN GP 120; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; MITOGENIC AGENT; PROTEIN P17; RIMONABANT; TETRAHYDROCANNABINOLIC ACID;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY RESPONSE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DRUG ACTIVITY; FEMALE; FETAL WELL BEING; FETUS; GESTATION PERIOD; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IN VITRO STUDY; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PERINATAL DRUG EXPOSURE; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; THYMOCYTE; THYMUS ATROPHY;

ANIMALS; APOPTOSIS; CASPASES; FEMALE; FETUS; HIV ANTIBODIES; HIV ANTIGENS; HIV-1; INDOLES; LYMPHOCYTE ACTIVATION; LYMPHOPOIESIS; MARIJUANA SMOKING; MICE; MICE, INBRED C57BL; PIPERIDINES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PSYCHOTROPIC DRUGS; PYRAZOLES; RECEPTORS, CANNABINOID; T-LYMPHOCYTES; TETRAHYDROCANNABINOL; THYMOCYTES; THYMUS GLAND;

EID: 80054782506     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.111.181206     Document Type: Article

References (45)

1. Azorlosa JL, Heishman SJ, Stitzer ML, and Mahaffey JM (1992) Marijuana smoking: effect of varying Δ9-tetrahydrocannabinol content and number of puffs. J Pharmacol Exp Ther 261:114-122.
2. Beal JE, Olson R, Laubenstein L, Morales JO, Bellman P, Yangco B, Lefkowitz L, Plasse TF, and Shepard KV (1995) Dronabinol as a treatment for anorexia associated with weight loss in patients with AIDS. J Pain Symptom Manage 10:89-97.
3. Berdyshev EV (2000) Cannabinoid receptors and the regulation of immune response. Chem Phys Lipids 108:169-190.
4. Bluhm EC, Daniels J, Pollock BH, Olshan AF, and Children's Oncology Group (United States) (2006) Maternal use of recreational drugs and neuroblastoma in offspring: a report from the Children's Oncology Group (United States). Cancer Causes Control 17:663-669. (Pubitemid 43668324)
5. Bonnin A, de Miguel R, Hernández ML, Ramos JA, and Fernández-Ruiz JJ (1995) The prenatal exposure to Δ9- tetrahydrocannabinol affects the gene expression and the activity of tyrosine hydroxylase during early brain development. Life Sci 56:2177-2184.
6. Brodbeck J, Matter M, and Moggi F (2006) Association between cannabis use and sexual risk behavior among young heterosexual adults. AIDS Behav 10:599-605. (Pubitemid 44285081)
7. Cabral GA and Dove Pettit DA (1998) Drugs and immunity: cannabinoids and their role in decreased resistance to infectious disease. J Neuroimmunol 83:116-123. (Pubitemid 28280957)
8. Camacho IA, Nagarkatti M, and Nagarkatti PS (2004) Evidence for induction of apoptosis in T cells from murine fetal thymus following perinatal exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol Sci 78:96-106. (Pubitemid 38351428)
9. Chan PC, Sills RC, Braun AG, Haseman JK, and Bucher JR (1996) Toxicity and carcinogenicity of Δ9-tetrahydrocannabinol in Fischer rats and B6C3F1 mice. Fundam Appl Toxicol 30:109-117.
10. del Arco I, Muñoz R, Rodríguez De Fonseca F, Escudero L, Martín-Calderón JL, Navarro M, and Villanúa MA (2000) Maternal exposure to the synthetic cannabinoid HU-210: effects on the endocrine and immune systems of the adult male offspring. Neuroimmunomodulation 7:16-26. (Pubitemid 30012575)
11. de Moraes Barros MC, Guinsburg R, de Araújo Peres C, Mitsuhiro S, Chalem E, and Laranjeira RR (2006) Exposure to marijuana during pregnancy alters neurobehavior in the early neonatal period. J Pediatr 149:781-787. (Pubitemid 44809271)
12. Do Y, McKallip RJ, Nagarkatti M, and Nagarkatti PS (2004) Activation through cannabinoid receptors 1 and 2 on dendritic cells triggers NF-κB-dependent apoptosis: novel role for endogenous and exogenous cannabinoids in immunoregulation. J Immunol 173:2373-2382. (Pubitemid 39063093)
13. Drumright LN, Little SJ, Strathdee SA, Slymen DJ, Araneta MR, Malcarne VL, Daar ES, and Gorbach PM (2006) Unprotected anal intercourse and substance use among men who have sex with men with recent HIV infection. J Acquir Immune Defic Syndr 43:344-350. (Pubitemid 44674016)
14. Fride E, Foox A, Rosenberg E, Faigenboim M, Cohen V, Barda L, Blau H, and Mechoulam R (2003) Milk intake and survival in newborn cannabinoid CB1 receptor knockout mice: evidence for a "CB3" receptor. Eur J Pharmacol 461: 27-34. (Pubitemid 36144261)
15. Fried PA, Watkinson B, and Willan A (1984) Marijuana use during pregnancy and decreased length of gestation. Am J Obstet Gynecol 150:23-27. (Pubitemid 14074594)
16. Haars R, Kronenberg M, Gallatin WM, Weissman IL, Owen FL, and Hood L (1986) Rearrangement and expression of T cell antigen receptor and γ genes during thymic development. J Exp Med 164:1-24. (Pubitemid 16069218)
17. Hegde VL, Hegde S, Cravatt BF, Hofseth LJ, Nagarkatti M, and Nagarkatti PS (2008) Attenuation of experimental autoimmune hepatitis by exogenous and endogenous cannabinoids: involvement of regulatory T cells. Mol Pharmacol 74:20-33. (Pubitemid 351872155)
18. Hegde VL, Nagarkatti M, and Nagarkatti PS (2010) Cannabinoid receptor activation leads to massive mobilization of myeloid-derived suppressor cells with potent immunosuppressive properties. Eur J Immunol 40:3358-3371.
19. Holladay SD (1999) Prenatal immunotoxicant exposure and postnatal autoimmune disease. Environ Health Perspect 107(Suppl 5):687-691.
20. Hurd YL, Wang X, Anderson V, Beck O, Minkoff H, and Dow-Edwards D (2005) Marijuana impairs growth in mid-gestation fetuses. Neurotoxicol Teratol 27:221-229. (Pubitemid 40279132)
21. Hutchings DE, Martin BR, Gamagaris Z, Miller N, and Fico T (1989) Plasma concentrations of Δ9-tetrahydrocannabinol in dams and fetuses following acute or multiple prenatal dosing in rats. Life Sci 44:697-701. (Pubitemid 19065969)
22. Johansson E, Norén K, Sjövall J, and Halldin MM (1989) Determination of Δ1- tetrahydrocannabinol in human fat biopsies from marihuana users by gas chromatography- mass spectrometry. Biomed Chromatogr 3:35-38. (Pubitemid 19036470)
23. Kamath AB, Xu H, Nagarkatti PS, and Nagarkatti M (1997) Evidence for the induction of apoptosis in thymocytes by 2,3,7,8-tetrachlorodibenzo-p-dioxin in vivo. Toxicol Appl Pharmacol 142:367-377. (Pubitemid 28381028)
24. Kingston R, Jenkinson EJ, and Owen JJ (1984) Characterization of stromal cell populations in the developing thymus of normal and nude mice. Eur J Immunol 14:1052-1056. (Pubitemid 15212229)
25. Klein TW, Newton CA, Nakachi N, and Friedman H (2000) Δ9-Tetrahydrocannabinol treatment suppresses immunity and early IFN-γ, IL-12, and IL-12 receptor β2responses to Legionella pneumophila infection. J Immunol 164:6461-6466. (Pubitemid 30408829)
26. Martin BR, Dewey WL, Harris LS, and Beckner JS (1977) 3H-Δ9-tetrahydrocannabinol distribution in pregnant dogs and their fetuses. Res Commun Chem Pathol Pharmacol 17:457-470. (Pubitemid 8146595)
27. McKallip RJ, Lombard C, Fisher M, Martin BR, Ryu S, Grant S, Nagarkatti PS, and Nagarkatti M (2002a) Targeting CB2 cannabinoid receptors as a novel therapy to treat malignant lymphoblastic disease. Blood 100:627-634. (Pubitemid 34761128)
28. 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.
29. McKallip RJ, Nagarkatti M, and Nagarkatti PS (2005) Δ9- Tetrahydrocannabinol enhances breast cancer growth and metastasis by suppression of the antitumor immune response. J Immunol 174:3281-3289. (Pubitemid 40354031)
30. Nagarkatti M, Rieder SA, Hegde VL, Kanada S, and Nagarkatti P (2010) Do cannabinoids have a therapeutic role in transplantation? Trends Pharmacol Sci 31:345-350.
31. Nagarkatti P, Pandey R, Rieder SA, Hegde VL, and Nagarkatti M (2009) Cannabinoids as novel anti-inflammatory drugs. Future Med Chem 1:1333-1349.
32. Pardoll DM, Fowlkes BJ, Bluestone JA, Kruisbeek A, Maloy WL, Coligan JE, and Schwartz RH (1987) Differential expression of two distinct T-cell receptors during thymocyte development. Nature 326:79-81. (Pubitemid 17059407)
33. Patrini G, Sacerdote P, Fuzio D, Manfredi B, and Parolaro D (1997) Regulation of immune functions in rat splenocytes after acute and chronic in vivo treatment with CP-55,940, a synthetic cannabinoid compound. J Neuroimmunol 80:143-148. (Pubitemid 28015334)
34. Reagan-Shaw S, Nihal M, and Ahmad N (2008) Dose translation from animal to human studies revisited. FASEB J 22:659-661. (Pubitemid 351348146)
35. Rieder SA, Chauhan A, Singh U, Nagarkatti M, and Nagarkatti P (2010) Cannabinoid-induced apoptosis in immune cells as a pathway to immunosuppression. Immunobiology 215:598-605.
36. Robison LL, Buckley JD, Daigle AE, Wells R, Benjamin D, Arthur DC, and Hammond GD (1989) Maternal drug use and risk of childhood nonlymphoblastic leukemia among offspring. An epidemiologic investigation implicating marijuana (a report from the Childrens Cancer Study Group). Cancer 63:1904-1911. (Pubitemid 19118887)
37. Roth MD, Tashkin DP, Whittaker KM, Choi R, and Baldwin GC (2005) Tetrahydrocannabinol suppresses immune function and enhances HIV replication in the huPBL-SCID mouse. Life Sci 77:1711-1722. (Pubitemid 41073664)
38. Sacerdote P, Massi P, Panerai AE, and 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.
39. Schwartz RH, Voth EA, and Sheridan MJ (1997) Marijuana to prevent nausea and vomiting in cancer patients: a survey of clinical oncologists. South Med J 90:167-172. (Pubitemid 27078730)
40. Urso P and Gengozian N (1984) Subnormal expression of cell-mediated and humoral immune responses in progeny disposed toward a high incidence of tumors after in utero exposure to benzo[a]pyrene. J Toxicol Environ Health 14:569-584. (Pubitemid 15191463)
41. Vela G, Fuentes JA, Bonnin A, Fernández-Ruiz J, and Ruiz-Gayo M (1995) Perinatal exposure to Δ9-tetrahydrocannabinol (Δ9-THC) leads to changes in opioid-related behavioral patterns in rats. Brain Res 680:142-147.
42. Vinner E, Vignau J, Thibault D, Codaccioni X, Brassart C, Humbert L, and Lhermitte M (2003) Neonatal hair analysis contribution to establishing a gestational drug exposure profile and predicting a withdrawal syndrome. Ther Drug Monit 25:421-432. (Pubitemid 36927972)
43. Voth EA and Schwartz RH (1997) Medicinal applications of Δ9-tetrahydrocannabinol and marijuana. Ann Intern Med 126:791-798.
44. Westfall RE, Janssen PA, Lucas P, and Capler R (2006) Survey of medicinal cannabis use among childbearing women: patterns of its use in pregnancy and retroactive self-assessment of its efficacy against 'morning sickness'. Complement Ther Clin Pract 12:27-33. (Pubitemid 43056765)
45. Zuckerman B, Frank DA, Hingson R, Amaro H, Levenson SM, Kayne H, Parker S, Vinci R, Aboagye K, and Fried LE (1989) Effects of maternal marijuana and cocaine use on fetal growth. N Engl J Med 320:762-768. (Pubitemid 19093542)