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Journal of Behavioral Medicine

, Volume 38, Issue 3, pp 527–534 | Cite as

Differential effects of self-reported lifetime marijuana use on interleukin-1 alpha and tumor necrosis factor in African American adults

  • Larry KeenIIEmail author
  • Arlener D. Turner
Article

Abstract

It is unknown how lifetime marijuana use affects different proinflammatory cytokines. The purpose of the current study is to explore potential differential effects of lifetime marijuana use on interleukin-1 alpha (IL-1α) and tumor necrosis factor (TNF) in a community based sample. Participants included 168 African American adults (51 % female, median age = 47 years). Upon study entry, blood was drawn and the participants completed questions regarding illicit drug use history whose answers were used to create three groups: lifetime non-drug users (n = 77), lifetime marijuana only users (n = 46) and lifetime marijuana and other drug users (n = 45). In the presence of demographic and physiological covariates, non-drug users were approximately two times more likely (AOR 2.73, CI 1.18, 6.31; p = .03) to have higher TNF levels than marijuana only users. Drug use was not associated with IL-1α. The influence of marijuana may be selective in nature, potentially localizing around innate immunity and the induction of cellular death.

Keywords

Marijuana Interleukin-1 Tumor necrosis factor African Americans Adults Immune function 

Notes

Acknowledgments

The parent study entitled Stress and Psychoneuroimmunological Factors in Renal Health and Disease, which is supported by a grant from the National Center for Minority Health and Health Disparities (P20 MD000512).

Conflict of interest

Larry Keen II and Arlener D. Turner, declare that they have no conflicts of interest.

Human and Animal Rights and Informed Consent

All procedures involving human participants in this study were performed in accordance with the ethical standards of the Howard University Institutional Review Board and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. In addition, informed consent was obtained from all individual participants prior to inclusion in the study.

References

  1. Aggarwal, S. K., Carter, G. T., Sullivan, M. D., ZumBrunnen, C., Morrill, R., & Mayer, H. D. (2009). Medicinal use of cannabis in the United States: Historical perspectives, current trends, and future. Journal of Opiod Management, 5, 153–168.Google Scholar
  2. Albayram, O., Alferink, J., Pitsch, J., Piyanova, A., Neitzert, K., Poppensieker, K.,… Bilkei-Gorzo, A. (2011). Role of CB1 cannabinoid receptors on GABAergic neurons in brain aging. Proceedings of the National Academy of Sciences of the United States of America, 108(27), 11256–11261. doi: 10.1073/pnas.1016442108
  3. Arevalo-Martin, A., Vela, J. M., Molina-Holgado, E., Borrell, J., & Guaza, C. (2003). Therapeutic action of cannabinoids in a murine model of multiple sclerosis. The Journal of Neuroscience, 23, 2511–2516.PubMedGoogle Scholar
  4. Baldwin, G. C., Tashkin, D. P., Buckley, D. M., Park, A. N., Dubinett, S. M., & Roth, M. D. (1997). Marijuana and cocaine impair alveolar macrophage function and cytokine production. American Journal of Respiratory and Critical Care Medicine, 156(5), 1606–1613. doi: 10.1164/ajrccm.156.5.9704146 CrossRefPubMedGoogle Scholar
  5. Black, P. H. (2003). The inflammatory response is an integral part of the stress response: Implications for atherosclerosis, insulin resistance, type II diabetes and metabolic syndrome X. Brain, Behavior, and Immunity, 17, 350–364.CrossRefPubMedGoogle Scholar
  6. Brady, K. T., & Randall, C. L. (1999). Gender differneces in substance use disorders. THe Psychiatric Clinics of North America, 22, 241–252.CrossRefPubMedGoogle Scholar
  7. Cabral, G. A., & Griffin-Thomas, L. (2009). Emerging role of the cannabinoid receptor CB2 in immune regulation: Therapeutic prospects for neuroinflammation. Expert Reviews in Molecular Medicine, 11, e3. doi: 10.1017/S1462399409000957 CrossRefPubMedCentralPubMedGoogle Scholar
  8. Cabral, G. A., & Vasquez, R. (1992). Delta-9-tetrahydrocannabinol suppresses macrophage extrinsic antiherpesvirus activity. Proceedings of the Society for Experimental Biology and Medicine, 199, 255–263.CrossRefPubMedGoogle Scholar
  9. Canvin, J. M., & el-Gabalawy, H. (1999). Anti-inflammatory therapy. Physical Medicine and Rehabilitation Clinics of North America, 10, 301–317.PubMedGoogle Scholar
  10. Chang, Y. H., Lee, S. T., & Lin, W. W. (2001). Effects of cannabinoids on LPS-stimulated inflammatory mediator release from macrophages: Involvement of eicosanoids. Journal of Cellular Biochemistry, 81, 715–723.CrossRefPubMedGoogle Scholar
  11. Degenhardt, L., Chiu, W., Sampson, N., Keslar, R. C., Anthony, J. C., Angemeyer, M., et al. (2008). Toward a global view of alcohol, tobacco, cannabis, and cocain use: Findings from the WHO World Mental Health Surveys. PLOS Medicine, 5, 1054–1067.CrossRefGoogle Scholar
  12. Feldman, A. M., Combs, A., Wagner, D., Kadakomi, T., Kubota, T., Li, Y. Y., & McTiernan, C. (2000). The role of tumor necrosis factor in the pathophysiology of heart failure. Journal of the American College of Cardiology, 35, 537–544.CrossRefPubMedGoogle Scholar
  13. Ferrucci, L., Corsi, A., Lauretani, F., Bandinelli, S., Bartali, B., Taub, Dennis, et al. (2005). Th origins of age-related proinflammaory state. Blood, 105, 2294–2299.CrossRefPubMedGoogle Scholar
  14. Fischer-Stenger, K., Dove Pettit, D. A., & Cabral, G. A. (1993). Delta 9-tetrahydrocannabinol inhibition of tumor necrosis factor-alpha: suppression of post-translational events. Journal of Pharmacology and Experimental Therapeutics, 267, 1558–1565.PubMedGoogle Scholar
  15. Friedman, H., & Klein, T. W. (1999). Marijuana and immunity. Science & Medicine, 6, 12–21.Google Scholar
  16. Glass, C. K., Saijo, K., Winner, B., Marchetto, M. C., & Gage, F. H. (2010). Mechanisms underlying inflammation in neurodegeneration. Cell, 140, 918–934. doi: 10.1016/j.cell.2010.02.016 CrossRefPubMedCentralPubMedGoogle Scholar
  17. Gorelick, P. B. (2010). Role of inflammation in cognitive impairment: results of observational epidemiological studies and clinical trials. Annals of the New York Academy of Sciences, 1207, 155–162. doi: 10.1111/j.1749-6632.2010.05726.x CrossRefPubMedGoogle Scholar
  18. Jackson, S. J., Diemel, L. T., Pryce, G., & Baker, D. (2005). Cannabinoids and neuroprotection in CNS inflammatory disease. Journal of the Neurological Sciences, 233, 21–25. doi: 10.1016/j.jns.2005.03.002 CrossRefPubMedGoogle Scholar
  19. Keatings, V. M., Collins, P. D., Scott, D. M., & Barnes, P. J. (1995). Differences in interleukin-8 and tumor necrosis factor-a in induced sputum from patients with chronic obstrudive pulmonary disease or asthma. American Journal of Respiratory and Critical Care Medicine, 153, 530–534.CrossRefGoogle Scholar
  20. Keen, L, 2nd, Pereira, D., & Latimer, W. (2014). Self-reported lifetime marijuana use and interleukin-6 levels in middle-aged African Americans. Drug and Alcohol Dependence. doi: 10.1016/j.drugalcdep.2014.04.011 PubMedGoogle Scholar
  21. Klein, T. W. (2005). Cannabinoid-based drugs as anti-inflammatory therapeutics. Nature Reviews Immunology, 5, 400–411. doi: 10.1038/nri1602 CrossRefPubMedGoogle Scholar
  22. Klein, T. W., Friedman, H., & Specter, S. (1998). Marijuana, immunity and infection. Journal of Neuroimmunology, 83, 102–115.CrossRefPubMedGoogle Scholar
  23. Klein, T. W., Lane, B., Newton, C. A., & Friedman, H. (2000). The cannabinoid system and cytokine network. Proceedings of the Society for Experimental Biology and Medicine, 225, 1–8.CrossRefPubMedGoogle Scholar
  24. Klein, T. W., Newton, C., Larsen, K., Lu, L., Perkins, I., Nong, L., & Friedman, H. (2003). The cannabinoid system and immune modulation. Journal of Leukocyte Biology, 74, 486–496. doi: 10.1189/jlb.0303101 CrossRefPubMedGoogle Scholar
  25. Kusher, D. I., Dawson, L. O., Taylor, A. C., & Djeu, J. Y. (1994). Effect of the psychoactive metabolite of marijuana, delta-9-tetrahydrocannabinol (THC), on the synthesis of tumor necrosis factor by human large granular lymphocytes. Cellular Immunology, 154, 99–108.CrossRefPubMedGoogle Scholar
  26. Levine, B., Kalman, J., Mayer, L., Fillit, H. M., & Packer, M. (1990). Elevated circulating levels of tumor necrosis factor in sever chronic heart failure. New England Journal of Medicine, 323, 236–241.CrossRefPubMedGoogle Scholar
  27. Li, G., Wang, L. Y., Shofer, J. B., Thompson, M. L., Peskind, E. R., McCormick, W.,… Larson, E. B. (2011). Temporal relationship between depression and dementia: findings from a large community-based 15-year follow-up study. Archives of General Psychiatry, 68(9), 970–977. doi: 10.1001/archgenpsychiatry.2011.86
  28. Maier, S. F., & Watkins, L. R. (1998). Cytokines for psychologists: implications of bidirectional immune-to-brain communication for understanding behavior, mood, and cognition. Psychological Review, 105, 83–107.CrossRefPubMedGoogle Scholar
  29. Marchetti, B., & Abbracchio, M. P. (2005). To be or not to be (inflamed)–is that the question in anti-inflammatory drug therapy of neurodegenerative disorders? Trends in Pharmacological Sciences, 26, 517–525. doi: 10.1016/j.tips.2005.08.007 CrossRefPubMedGoogle Scholar
  30. Matsuda, K., Mikami, Y., Takeda, K., Fukuyama, S., Egawa, S., Sunamura, M.,… Matsuno, S. (2005). The cannabinoid 1 receptor antagonist, AM251, prolongs the survival of rats with severe acute pancreatitis. Tohoku Journal of Experimental Medicine, 207(2), 99–107.Google Scholar
  31. McDade, T. W., Hawkley, L. C., & Cacioppo, J. T. (2006). Psychosocial and behavioral predictors of inflammation in middle-aged and older adults: The Chicago health, aging, and social relations study. Psychosomatic Medicine, 68, 376–381. doi: 10.1097/01.psy.0000221371.43607.64 CrossRefPubMedGoogle Scholar
  32. Mohamed-Ali, V., Goodrick, S., Rawesh, A., Katz, D. R., Miles, J. M., Yudkin, J. S.,… Coppack, S. W. (1997). Subcutaneous adipose tissue releases interleukin-6, but not tumor necrosis factor-alpha, in vivo. Journal of Clinical Endocrinology and Metabolism, 82(12), 4196–4200. doi: 10.1210/jcem.82.12.4450
  33. O’Mahony, L., Holland, J., Jackson, J., Feighery, C., Hennessy, T. P. J., & Mealy, K. (1998). Quantitative intracellular cytokine measuremnet: age-related changes in proinflammatory cytokine production. Clinical and Experimental Immunology, 113, 213–219.CrossRefPubMedCentralPubMedGoogle Scholar
  34. Prenninx, B. W. H., Kritchevsky, S. B., Yaffe, K., Newman, A. B., Simonsick, E. M., Rubin, S.,… Pahor, M. (2003). Inflammatory markers and depressed mood in older persons: Results from the health, aging and body composition study. Biological Psychiatry, 54, 566–572. doi: 10.1016/S0006-3223(02)01811-5
  35. Raber, J., Sorg, O., Horn, T. F., Yu, N., Koob, G. F., Campbell, I. L., & Bloom, F. E. (1998). Inflammatory cytokines: putative regulators of neuronal and neuro-endocrine function. Brain Research. Brain Research Reviews, 26, 320–326.CrossRefPubMedGoogle Scholar
  36. Reiss, C. S. (2010). Cannabinoids and viral infections. Pharmaceuticals (Basel, Switzerland), 3(6), 1873–1886. doi: 10.3390/ph3061873
  37. Ribeiro, A., Ferraz-de-Paula, V., Pinheiro, M. L., Vitoretti, L. B., Mariano-Souza, D. P., Quinteiro-Filho, W. M.,… Palermo-Neto, J. (2012). Cannabidiol, a non-psychotropic plant-derived cannabinoid, decreases inflammation in a murine model of acute lung injury: role for the adenosine A(2A) receptor. European Journal of Pharmacology, 678(1–3), 78–85. doi: 10.1016/j.ejphar.2011.12.043
  38. Roth, M. D., Baldwin, G. C., & Tashkin, D. P. (2002). Effects of delta-9-tetrahydrocannabinol on human immune function and host defense. Chemistry and Physics of Lipids, 121, 229–239.CrossRefPubMedGoogle Scholar
  39. Roux-Lombard, P., Modoux, C., Cruchaud, A., & Dayer, J. (1989). Purified Blood Monocytes from HIV 1-infected patients produce high levels of TNFa and IL-1. Clinical Immunology and Immunopathology, 50, 374–384.CrossRefPubMedGoogle Scholar
  40. Shivers, S. C., Newton, C., FRiedman, H., & Klein, T. W. (1994). Delta-9-tetrahydrocannabinol (THC) modulates IL-1 bioactivity in human monocyte/macrophage cell lines. Life Sciences, 54, 1281–1289.CrossRefPubMedGoogle Scholar
  41. Snella, E., Pross, S., & Friedman, H. (1995). Relationship of Aging and Cytokines to the immunomodulation by delta-9-tetrahydrocannabinol on murine lymphoid cells. International Society fo Immunopharmacology, 17, 1045–1054.CrossRefGoogle Scholar
  42. Sperry, J. L., Friese, R. S., Frankel, H. L., West, M. A., Cuschieri, J., Moore, E. E., et al. (2008). Male gender is associated with excessive IL-6 expression following severe injury. Journal of Trauma, 64, 572–578.CrossRefPubMedGoogle Scholar
  43. Stowe, R. P., Peek, M. K., Cutchin, M. P., & Goodwin, J. S. (2010). Plasma cytokine levels in a population-based study: Relation to age and ethnicity. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 65A, 429–433.CrossRefGoogle Scholar
  44. Testa, M., Yeh, M., Lee, P., Fanelli, R., Loperfido, F., Berman, J. W., & LeJemetel, T. H. (1996). Circulating levels of cytokines and their endogenous modulators in patients with mild to severe congestive heart failure due to coronary artery disease or hypertension. Journal of the American College of Cardiology, 28, 964–971.CrossRefPubMedGoogle Scholar
  45. Yang, Y. S., Lim, H. K., Hong, K. K., Shin, M. K., Lee, J. W., Lee, S. W., & Kim, N. I. (2014). Cigarette smoke-induced interleukin-1 alpha may be involved in the pathogenesis of adult acne. Ann Dermatol, 26, 11–16. doi: 10.5021/ad.2014.26.1.11 CrossRefPubMedCentralPubMedGoogle Scholar
  46. Zurier, R. B., Rossetti, R. G., Burstein, S. H., & Bidinger, B. (2003). Suppression of human monocyte interleukin-1beta production by ajulemic acid, a nonpsychoactive cannabinoid. Biochemical Pharmacology, 65, 649–655.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Department of PsychologyVirginia State UniversityPetersburgUSA
  2. 2.Center of Excellence on Disparities in HIV and AgingRush University Medical CenterChicagoUSA

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