Journal of Neuroimmune Pharmacology

, Volume 10, Issue 2, pp 217–232 | Cite as

Behavioral, Metabolic, and Immune Consequences of Chronic Alcohol or Cannabinoids on HIV/AIDs: Studies in the Non-Human Primate SIV Model

  • Patricia E. MolinaEmail author
  • Angela M. Amedee
  • Peter Winsauer
  • Steve Nelson
  • Gregory Bagby
  • Liz Simon


HIV-associated mortality has been significantly reduced with antiretroviral therapy (ART), and HIV infection has become a chronic disease that frequently coexists with many disorders, including substance abuse (Azar et al. Drug Alcohol Depend 112:178–193, 2010; Phillips et al. J Gen Int Med 16:165, 2001). Alcohol and drugs of abuse may modify host-pathogen interactions at various levels including behavioral, metabolic, and immune consequences of HIV infection, as well as the ability of the virus to integrate into the genome and replicate in host cells. Identifying mechanisms responsible for these interactions is complicated by many factors, such as the tissue specific responses to viral infection, multiple cellular mechanisms involved in inflammatory responses, neuroendocrine and localized responses to infection, and kinetics of viral replication. An integrated physiological analysis of the biomedical consequences of chronic alcohol and drug use or abuse on disease progression is possible using rhesus macaques infected with simian immunodeficiency virus (SIV), a relevant model of HIV infection. This review will provide an overview of the data gathered using this model to show that chronic administration of two of the most commonly abused substances, alcohol and cannabinoids (Δ9-Tetrahydrocannabinol; THC), affect host-pathogen interactions.


HIV SIV Alcohol Cannabinoids Immune system Metabolism 



The authors are grateful for the outstanding veterinarian and technical support provided by Jason Dufour, DVM, Leslie Birke, DVM, Jean Carnal, Connie Porretta, Curtis Vande Stouwe, Rhonda Martinez, Amy Weinberg, Peter Lewis, and Jamie Hubbell. Analytical support for the studies was provided by the LSUHSC Comprehensive Alcohol Research Center Analytical Core Laboratory, and particularly Dr. Robert Siggins.


The authors have received support from: NIH/NIAAA P60 AA09803, NIH/NIDA 5 R01 DA030053.

Conflicts of Interest

The authors declare no conflicts of interest.


  1. Abrams DI et al (2003) Short-term effects of cannabinoids in patients with HIV-1 infection: a randomized, placebo-controlled clinical trial. Ann Intern Med 139:258–266PubMedGoogle Scholar
  2. ADAMP NIoJ (2003) Drug and alcohol use & related matters among arrestees. Washington DCGoogle Scholar
  3. Adaramoye OA, Oloyede GK (2012) Effect of moderate ethanol administration on biochemical indices in streptozotocin-diabetic Wistar rats. West Indian Med J 61:3–9PubMedGoogle Scholar
  4. Addolorato G et al (2000) Body composition changes induced by chronic ethanol abuse: evaluation by dual energy X-ray absorptiometry. Am J Gastroenterol 95:2323–2327. doi: 10.1111/j.1572-0241.2000.02320.x PubMedGoogle Scholar
  5. Amedee AM et al (2014a) Chronic delta-tetrahydrocannabinol administration may not attenuate simian immunodeficiency virus disease progression in female rhesus macaques. AIDS Res Hum Retrovir. doi: 10.1089/AID.2014.0108 Google Scholar
  6. Amedee AM, Veazey R, Molina P, Nelson S, Bagby GJ (2014b) Chronic binge alcohol increases susceptibility to rectal simian immunodeficiency virus infection in macaques. AIDS 28:2485–2487. doi: 10.1097/qad.0000000000000413 PubMedGoogle Scholar
  7. Arthur LO, Gilden RV, Marx PA, Gardner MB (1986) Simian acquired immunodeficiency syndrome. Progr Alerg 37:332–352Google Scholar
  8. Azar MM, Springer SA, Meyer JP, Altice FL (2010) A systematic review of the impact of alcohol use disorders on HIV treatment outcomes, adherence to antiretroviral therapy and health care utilization. Drug Alcohol Depend 112:178–193. doi: 10.1016/j.drugalcdep.2010.06.014, PMCID: PMC2997193PubMedCentralPubMedGoogle Scholar
  9. Bagasra O et al (1996) Increased human immunodeficiency virus type 1 replication in human peripheral blood mononuclear cells induced by ethanol: potential immunopathogenic mechanisms. J Infect Dis 173:550–558PubMedGoogle Scholar
  10. Bagby GJ, Zhang P, Purcell JE, Didier PJ, Nelson S (2006) Chronic binge ethanol consumption accelerates progression of simian immunodeficiency virus disease. Alcohol Clin Exp Res 30:1781–1790PubMedGoogle Scholar
  11. Baliunas DO, Taylor BJ, Irving H, Roerecke M, Patra J, Mohapatra S, Rehm J (2009) Alcohol as a risk factor for type 2 diabetes: a systematic review and meta-analysis. Diabetes Care 32:2123–2132. doi: 10.2337/dc09-0227, PMCID: PMC2768203PubMedCentralPubMedGoogle Scholar
  12. Barbaro G (2006) Highly active antiretroviral therapy-associated metabolic syndrome: pathogenesis and cardiovascular risk. Am J Ther 13:248–260. doi: 10.1097/01.mjt.0000162013.66614.16 PubMedGoogle Scholar
  13. Baskin GB, Murphey-Corb M, Watson EA, Martin LN (1988) Necropsy findings in rhesus monkeys experimentally infected with cultured simian immunodeficiency virus (SIV)/delta. Vet Pathol 25:456–467PubMedGoogle Scholar
  14. Bau PF, Bau CH, Rosito GA, Manfroi WC, Fuchs FD (2007) Alcohol consumption, cardiovascular health, and endothelial function markers. Alcohol 41:479–488. doi: 10.1016/j.alcohol.2007.08.004 PubMedGoogle Scholar
  15. Baum MK, Rafie C, Lai S, Sales S, Page JB, Campa A (2010) Alcohol use accelerates HIV disease progression. AIDS Res Hum Retrovir 26:511–518. doi: 10.1089/aid.2009.0211, PMCID: PMC2875959PubMedCentralPubMedGoogle Scholar
  16. Bell JE, Brettle RP, Chiswick A, Simmonds P (1998) HIV encephalitis, proviral load and dementia in drug users and homosexuals with AIDS. effect of neocortical involvement. Brain : J Neurol 121(Pt 11):2043–2052Google Scholar
  17. Beulens JW et al (2012) Alcohol consumption and risk of type 2 diabetes in European men and women: influence of beverage type and body size. the EPIC-InterAct study. J Intern Med 272:358–370. doi: 10.1111/j.1365-2796.2012.02532.x PubMedGoogle Scholar
  18. Bing EG et al (2001) Psychiatric disorders and drug use among human immunodeficiency virus-infected adults in the United States. Arch Gen Psychiatry 58:721–728PubMedGoogle Scholar
  19. Boden G, Chen X, DeSantis RA, Kendrick Z (1993) Ethanol inhibits insulin action on lipolysis and on insulin release in elderly men. AM j Physiol 265:E197–E202PubMedGoogle Scholar
  20. Braitstein P, Kendall T, Chan K, Wood E, Montaner JS, O’Shaughnessy MV, Hogg RS (2001) Mary-Jane and her patients: sociodemographic and clinical characteristics of HIV-positive individuals using medical marijuana and antiretroviral agents. Aids 15:532–533PubMedGoogle Scholar
  21. Brenchley JM et al (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12:1365–1371. doi: 10.1038/nm1511 PubMedGoogle Scholar
  22. Bunout D (1999) Nutritional and metabolic effects of alcoholism: their relationship with alcoholic liver disease. Nutrition 15:583–589PubMedGoogle Scholar
  23. Cabral GA, Stinnett AL, Bailey J, Ali SF, Paule MG, Scallet AC, Slikker W Jr (1991) Chronic marijuana smoke alters alveolar macrophage morphology and protein expression. Pharmacol Biochem Behav 40:643–649PubMedGoogle Scholar
  24. Carlini EA (2004) The good and the bad effects of (-) trans-delta-9-tetrahydrocannabinol (Delta 9-THC) on humans. Toxicon : Off J Int Soc Toxinol 44:461–467. doi: 10.1016/j.toxicon.2004.05.009 Google Scholar
  25. Carr A, Cooper DA (2000) Adverse effects of antiretroviral therapy. Lancet 356:1423–1430. doi: 10.1016/S0140-6736(00)02854-3 PubMedGoogle Scholar
  26. Carr A, Samaras K, Burton S, Law M, Freund J, Chisholm DJ, Cooper DA (1998) A syndrome of peripheral lipodystrophy, hyperlipidaemia and insulin resistance in patients receiving HIV protease inhibitors. AIDS 12:F51–F58PubMedGoogle Scholar
  27. Centers for Disease Control and Prevention (2014) Monitoring selected national HIV prevention and care objectives by using HIV surveillance data—United States and 6 dependent areas—2012. HIV Surveillance Supplemental Report 2014;19(No.3)Google Scholar
  28. Chandra LC et al. (2014) Chronic administration of Δ9-Tetrahydrocannabinol induces intestinal anti-inflammatory microRNA expression during acute SIV infection of rhesus macaques Journal of Virology. PMCID: PMCJournal - In ProcessGoogle Scholar
  29. Chen X, Sebastian BM, Nagy LE (2007) Chronic ethanol feeding to rats decreases adiponectin secretion by subcutaneous adipocytes. Am J Physiol Endocrinol Metab 292:E621–E628. doi: 10.1152/ajpendo.00387.2006, PMCID: PMC1794258PubMedCentralPubMedGoogle Scholar
  30. Cheney PD, Riazi M, Marcario JM (2008) Behavioral and neurophysiological hallmarks of simian immunodeficiency virus infection in macaque monkeys. J Neurovirol 14:301–308. doi: 10.1080/13550280802116322 PubMedGoogle Scholar
  31. Cheng DM, Libman H, Bridden C, Saitz R, Samet JH (2009) Alcohol consumption and lipodystrophy in HIV-infected adults with alcohol problems. Alcohol 43:65–71. doi: 10.1016/j.alcohol.2008.09.004, PMCID: PMC2635495PubMedCentralPubMedGoogle Scholar
  32. Chitsaz E (2013) Contribution of substance use disorders on HIV treatment outcomes and antiretroviral medication adherence among HIV-infected persons entering jail. AIDS Behav 17(Suppl 2):S118–S127. doi: 10.1007/s10461-013-0506-0, PMCID: PMC3818019PubMedGoogle Scholar
  33. Cinti S (2009) Medical marijuana in HIV-positive patients: what do we know? J Int Assoc Phys AIDS Care (Chic) 8:342–346. doi: 10.1177/1545109709351167 Google Scholar
  34. Conigrave KM, Rimm EB (2003) Alcohol for the prevention of type 2 diabetes mellitus? Treat Endocrinol 2:145–152PubMedGoogle Scholar
  35. Coskun ZM, Bolkent S (2014) Oxidative stress and cannabinoid receptor expression in type-2 diabetic rat pancreas following treatment with Delta(9) -THC. Cell Biochem Funct 32:612–619. doi: 10.1002/cbf.3058 PubMedGoogle Scholar
  36. Costantino CM, Gupta A, Yewdall AW, Dale BM, Devi LA, Chen BK (2012) Cannabinoid receptor 2-mediated attenuation of CXCR4-tropic HIV infection in primary CD4+ T cells. PLoS One 7:10.1371/journal.pone.0033961. doi: 10.1371/journal.pone.0033961, PMCID: PMC3309010Google Scholar
  37. Cysique LA, Brew BJ (2009) Neuropsychological functioning and antiretroviral treatment in HIV/AIDS: a review. Neuropsychol Rev 19:169–185. doi: 10.1007/s11065-009-9092-3 PubMedGoogle Scholar
  38. Czaja JA (1975) Food rejection by female rhesus monkeys during the menstrual cycle and early pregnancy. Physiol Behav 14:579–587PubMedGoogle Scholar
  39. da Cunha A, Eiden LE, Rausch DM (1994) Neuronal substrates for SIV encephalopathy. Adv Neuroimmunol 4:265–271PubMedGoogle Scholar
  40. Daniel JM, Winsauer PJ, Brauner IN, Moerschbaecher JM (2002) Estrogen improves response accuracy and attenuates the disruptive effects of delta9-THC in ovariectomized rats responding under a multiple schedule of repeated acquisition and performance. Behav Neurosci 116:989–998PubMedGoogle Scholar
  41. Daul CB, Heath RG (1975) The effect of chronic marihuana usage on the immunological status of rheusus monkeys. Life Sci 17:875–881PubMedGoogle Scholar
  42. de la Monte S, Derdak Z, Wands JR (2012) Alcohol, insulin resistance and the liver-brain axis. J Gastroenterol Hepatol 27(Suppl 2):33–41. doi: 10.1111/j.1440-1746.2011.07023.x PubMedGoogle Scholar
  43. Deveaux L et al (2007) Reduction in human immunodeficiency virus risk among youth in developing countries. Arch Pediatr Adolesc Med 161:1130–1139. doi: 10.1001/archpedi.161.12.1130 PubMedGoogle Scholar
  44. Dewey WL (1986) Cannabinoid pharmacology. Pharmacol Rev 38:151–178PubMedGoogle Scholar
  45. Di Marzo V (2008) The endocannabinoid system in obesity and type 2 diabetes. Diabetologia 51:1356–1367. doi: 10.1007/s00125-008-1048-2 PubMedGoogle Scholar
  46. Diaz S, Farhang B, Hoien J, Stahlman M, Adatia N, Cox JM, Wagner EJ (2009) Sex differences in the cannabinoid modulation of appetite, body temperature and neurotransmission at POMC synapses. Neuroendocrinology 89:424–440. doi: 10.1159/000191646 PubMedGoogle Scholar
  47. Ehrhart J (2005) Stimulation of cannabinoid receptor 2 (CB2) suppresses microglial activation. J Neuroinflammation 2:29. doi: 10.1186/1742-2094-2-29, PMCID: PMC1352348PubMedCentralPubMedGoogle Scholar
  48. Eisner V, Lenaers G, Hajnoczky G (2014) Mitochondrial fusion is frequent in skeletal muscle and supports excitation-contraction coupling. J Cell Biol 205:179–195. doi: 10.1083/jcb.201312066, PMCID: PMC4003250PubMedCentralPubMedGoogle Scholar
  49. ElSohly MA, deWit H, Wachtel SR, Feng S, Murphy TP (2001) Delta9-tetrahydrocannabivarin as a marker for the ingestion of marijuana versus Marinol: results of a clinical study. J Anal Toxicol 25:565–571PubMedGoogle Scholar
  50. Engeli S et al (2005) Activation of the peripheral endocannabinoid system in human obesity. Diabetes 54:2838–2843, PMCID: PMC2228268PubMedCentralPubMedGoogle Scholar
  51. Fama R et al (2007) Upper and lower limb motor impairments in alcoholism. HIV infection, and their comorbidity. Alcohol Clin Exp Res 31:1038–1044. doi: 10.1111/j.1530-0277.2007.00385.x PubMedGoogle Scholar
  52. Fattore L, Fratta W (2010) How important are sex differences in cannabinoid action? Br J Pharmacol 160:544–548. doi: 10.1111/j.1476-5381.2010.00776.x, PMCID: PMC2931555PubMedCentralPubMedGoogle Scholar
  53. Fein G, Biggins CA, MacKay S (1995) Alcohol abuse and HIV infection have additive effects on frontal cortex function as measured by auditory evoked potential P3A latency. Biol Psychiatry 37:183–195. doi: 10.1016/0006-3223(94)00119-n PubMedGoogle Scholar
  54. Felder CC et al (1996) Isolation and measurement of the endogenous cannabinoid receptor agonist, anandamide, in brain and peripheral tissues of human and rat. FEBS Lett 393:231–235PubMedGoogle Scholar
  55. Fernandez-Sola J, Nicolas JM, Sacanella E, Robert J, Cofan M, Estruch R, Urbano-Marquez A (2000) Low-dose ethanol consumption allows strength recovery in chronic alcoholic myopathy. QJM : Month J Assoc Phys 93:35–40Google Scholar
  56. Filipeanu CM, Guidry JJ, Leonard ST, Winsauer PJ (2011) Delta9-THC increases endogenous AHA1 expression in rat cerebellum and may modulate CB1 receptor function during chronic use. J Neurochem 118:1101–1112. doi: 10.1111/j.1471-4159.2011.07391.x PubMedGoogle Scholar
  57. Friedman H, Klein TW, Newton C, Daaka Y (1995) Marijuana, receptors and immunomodulation. Adv Exp Med Biol 373:103–113PubMedGoogle Scholar
  58. Furler MD, Einarson TR, Millson M, Walmsley S, Bendayan R (2004) Medicinal and recreational marijuana use by patients infected with HIV. AIDS Patient Care STDS 18:215–228. doi: 10.1089/108729104323038892 PubMedGoogle Scholar
  59. Galvan FH et al (2002) The prevalence of alcohol consumption and heavy drinking among people with HIV in the United States: results from the HIV cost and services utilization study. J Stud Alcohol 63:179–186PubMedGoogle Scholar
  60. Gao L et al (2010) Chronic ethanol consumption up-regulates protein-tyrosine phosphatase-1B (PTP1B) expression in rat skeletal muscle. Acta Pharmacol Sin 31:1576–1582. doi: 10.1038/aps.2010.161, PMCID: PMC4002945PubMedCentralPubMedGoogle Scholar
  61. Gardner MB, Luciw PA (1988) Simian immunodeficiency viruses and their relationship to the human immunodeficiency viruses. Aids 2(Suppl 1):S3–S10PubMedGoogle Scholar
  62. Ghosn J et al (2014) HIV-1 DNA levels in peripheral blood mononuclear cells and cannabis use are associated with intermittent HIV shedding in semen of men who have sex with men on successful antiretroviral regimens. Clin Infect Dis 58:1763–1770. doi: 10.1093/cid/ciu187 PubMedGoogle Scholar
  63. Gold LH et al (1998) Longitudinal analysis of behavioral, neurophysiological, viral and immunological effects of SIV infection in rhesus monkeys. J Med Primatol 27:104–112PubMedGoogle Scholar
  64. Gonzalez S et al (2000) Sex steroid influence on cannabinoid CB(1) receptor mRNA and endocannabinoid levels in the anterior pituitary gland. Biochem Biophys Res Commun 270:260–266. doi: 10.1006/bbrc.2000.2406 PubMedGoogle Scholar
  65. Grant I (1987) Alcohol and the brain: neuropsychological correlates. J Consult Clin Psychol 55:310–324PubMedGoogle Scholar
  66. Grant I, Heaton RK, Atkinson JH (1995) Neurocognitive disorders in HIV-1 infection. HNRC Group HIV Neurobehavioral Research Center. Curr Topic Microbiol Immunol 202:11–32Google Scholar
  67. Green JE, Saveanu RV, Bornstein RA (2004) The effect of previous alcohol abuse on cognitive function in HIV infection. Am J Psychiatry 161:249–254PubMedGoogle Scholar
  68. Grinspoon S et al (1997) Body composition and endocrine function in women with acquired immunodeficiency syndrome wasting. J Clin Endocrinol Metab 82:1332–1337. doi: 10.1210/jcem.82.5.3907 PubMedGoogle Scholar
  69. Gutierrez AD, Balasubramanyam A (2012) Dysregulation of glucose metabolism in HIV patients: epidemiology, mechanisms, and management. Endocrine 41:1–10. doi: 10.1007/s12020-011-9565-z, PMCID: PMC3417129PubMedCentralPubMedGoogle Scholar
  70. Hadigan C, Corcoran C, Stanley T, Piecuch S, Klibanski A, Grinspoon S (2000) Fasting hyperinsulinemia in human immunodeficiency virus-infected men: relationship to body composition, gonadal function, and protease inhibitor use. J Clin Endocrinol Metab 85:35–41. doi: 10.1210/jcem.85.1.6264 PubMedGoogle Scholar
  71. Hampson RE, Deadwyler SA (1999) Cannabinoids, hippocampal function and memory. Life Sci 65:715–723PubMedGoogle Scholar
  72. Hampson RE, Deadwyler SA (2000) Cannabinoids reveal the necessity of hippocampal neural encoding for short-term memory in rats. J Neurosci : Off J Soc Neurosci 20:8932–8942Google Scholar
  73. Haney M, Gunderson EW, Rabkin J, Hart CL, Vosburg SK, Comer SD, Foltin RW (2007) Dronabinol and marijuana in HIV-positive marijuana smokers. caloric intake, mood, and sleep. J Acquir Immune Defic Syndr 45:545–554. doi: 10.1097/QAI.0b013e31811ed205 PubMedGoogle Scholar
  74. Harris GE (2014) Patterns and correlates of cannabis use among individuals with HIV/AIDS in Maritime Canada. Can J Infect Dis Med Microbiol = J Canadien des maladies infectieuses et de la Microbiol Med / AMMI Can 25:e1–e7, PMCID: PMC3950986Google Scholar
  75. Harvey BS, Nicotra LL, Vu M, Smid SD (2013) Cannabinoid CB2 receptor activation attenuates cytokine-evoked mucosal damage in a human colonic explant model without changing epithelial permeability. Cytokine 63:209–217. doi: 10.1016/j.cyto.2013.04.032 PubMedGoogle Scholar
  76. Hayatbakhsh MR, O’Callaghan MJ, Mamun AA, Williams GM, Clavarino A, Najman JM (2010) Cannabis use and obesity and young adults. Am J Drug Alcohol Abuse 36:350–356. doi: 10.3109/00952990.2010.500438 PubMedGoogle Scholar
  77. Hendershot CS, Stoner SA, George WH, Norris J (2007) Alcohol use, expectancies, and sexual sensation seeking as correlates of HIV risk behavior in heterosexual young adults. Psychol Addict Behav 21:365–372. doi: 10.1037/0893-164X.21.3.365, PMCID: PMC2749924PubMedCentralPubMedGoogle Scholar
  78. Heyes MP et al (1992) Relationship of neurologic status in macaques infected with the simian immunodeficiency virus to cerebrospinal fluid quinolinic acid and kynurenic acid. Brain Res 570:237–250PubMedGoogle Scholar
  79. Hollister LE (1986) Health aspects of cannabis. Pharmacol Rev 38:1–20PubMedGoogle Scholar
  80. Horvath B, Mukhopadhyay P, Hasko G, Pacher P (2012) The endocannabinoid system and plant-derived cannabinoids in diabetes and diabetic complications. Am J Pathol 180:432–442. doi: 10.1016/j.ajpath.2011.11.003, PMCID: PMC3349875PubMedCentralPubMedGoogle Scholar
  81. Howard AA, Arnsten JH, Gourevitch MN (2004) Effect of alcohol consumption on diabetes mellitus: a systematic review. Ann Intern Med 140:211–219PubMedGoogle Scholar
  82. Hunault CC et al (2009) Cognitive and psychomotor effects in males after smoking a combination of tobacco and cannabis containing up to 69 mg delta-9-tetrahydrocannabinol (THC). Psychopharmacology 204:85–94. doi: 10.1007/s00213-008-1440-0 PubMedGoogle Scholar
  83. Ivashkiv LB, Donlin LT (2014) Regulation of type I interferon responses. nature reviews. Immunology 14:36–49. doi: 10.1038/nri3581, PMCID: PMC4084561PubMedCentralPubMedGoogle Scholar
  84. Jarvis CM, Hayman LL, Braun LT, Schwertz DW, Ferrans CE, Piano MR (2007) Cardiovascular risk factors and metabolic syndrome in alcohol- and nicotine-dependent men and women. J Cardiovasc Nurs 22:429–435. doi: 10.1097/01.JCN.0000297387.21626.88 PubMedGoogle Scholar
  85. Jones CY et al (2005) Insulin resistance in HIV-infected men and women in the nutrition for healthy living cohort. J Acquir Immune Defic Syndr 40:202–211PubMedGoogle Scholar
  86. Kadowaki T, Yamauchi T, Kubota N, Hara K, Ueki K, Tobe K (2006) Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J Clin Invest 116:1784–1792. doi: 10.1172/jci29126, PMCID: PMCPmc1483172PubMedCentralPubMedGoogle Scholar
  87. Kamin DS, Grinspoon SK (2005) Cardiovascular disease in HIV-positive patients. AIDS 19:641–652PubMedGoogle Scholar
  88. Khalsa JH, Royal W (2004) Do drugs of abuse impact on HIV disease? J Neuroimmunol 147:6–8PubMedGoogle Scholar
  89. Kino T, Chrousos GP (2003) AIDS-related insulin resistance and lipodystrophy syndrome. Curr Drug Targ Imm, Endocrine Metab Disord 3:111–117Google Scholar
  90. Klatsky AL (2007) Alcohol, cardiovascular diseases and diabetes mellitus. Pharmacol Res : Off J Italian Pharmacol Soc 55:237–247. doi: 10.1016/j.phrs.2007.01.011 Google Scholar
  91. Klein TW, 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. doi: 10.1189/jlb.0303101 PubMedGoogle Scholar
  92. Kolter DP (2003) Current concepts of metabolic abnormalities in HIV patients: focus on lipodystrophy. AIDS Read 13:S5–S13PubMedGoogle Scholar
  93. Kotler DP, Wang J, Pierson RN (1985) Body composition studies in patients with the acquired immunodeficiency syndrome. Am J Clin Nutri 42:1255–1265Google Scholar
  94. Kumar R et al (2005) Increased viral replication in simian immunodeficiency virus/simian-HIV-infected macaques with self-administering model of chronic alcohol consumption. J Acquir Immune Defic Syndr 39:386–390PubMedGoogle Scholar
  95. Lackner AA, Veazey RS (2007) Current concepts in AIDS pathogenesis: insights from the SIV/macaque model. Annu Rev Med 58:461–476. doi: 10.1146/ PubMedGoogle Scholar
  96. Landfield PW, Cadwallader LB, Vinsant S (1988) Quantitative changes in hippocampal structure following long-term exposure to delta 9-tetrahydrocannabinol: possible mediation by glucocorticoid systems. Brain Res 443:47–62PubMedGoogle Scholar
  97. Lang CH, Kimball SR, Frost RA, Vary TC (2001) Alcohol myopathy: impairment of protein synthesis and translation initiation. Int J Biochem Cell Biol 33:457–473PubMedGoogle Scholar
  98. Lang CH, Frost RA, Summer AD, Vary TC (2005) Molecular mechanisms responsible for alcohol-induced myopathy in skeletal muscle and heart. Int J Biochem Cell Biol 37:2180–2195. doi: 10.1016/j.biocel.2005.04.013 PubMedGoogle Scholar
  99. Le Foll B, Trigo JM, Sharkey KA, Le Strat Y (2013) Cannabis and Delta9-tetrahydrocannabinol (THC) for weight loss? Med Hypotheses 80:564–567. doi: 10.1016/j.mehy.2013.01.019 PubMedGoogle Scholar
  100. Le Strat Y, Le Foll B (2011) Obesity and cannabis use: results from 2 representative national surveys. Am J Epidemiol 174:929–933. doi: 10.1093/aje/kwr200 PubMedGoogle Scholar
  101. LeCapitaine NJ et al (2011) Disrupted anabolic and catabolic processes may contribute to alcohol-accentuated SAIDS-associated wasting. J Infect Dis 204:1246–1255. doi: 10.1093/infdis/jir508, PMCID: PMC3173505PubMedCentralPubMedGoogle Scholar
  102. Lee LM, Karon JM, Selik R, Neal JJ, Fleming PL (2001) Survival after AIDS diagnosis in adolescents and adults during the treatment era, United States 1984–1997. Jama 285:1308–1315PubMedGoogle Scholar
  103. Leggio L et al (2009) Is cortisol involved in the alcohol-related fat mass impairment? a longitudinal clinical study. Alcohol Alcohol 44:211–215. doi: 10.1093/alcalc/agn116 PubMedGoogle Scholar
  104. Letvin NL (1990) Animal models for AIDS. Immunol Today 11:322–326PubMedGoogle Scholar
  105. Li X, Kaminski NE, Fischer LJ (2001) Examination of the immunosuppressive effect of delta9-tetrahydrocannabinol in streptozotocin-induced autoimmune diabetes. Int Immunopharmacol 1:699–712PubMedGoogle Scholar
  106. Lichtman AH, Dimen KR, Martin BR (1995) Systemic or intrahippocampal cannabinoid administration impairs spatial memory in rats. Psychopharmacology 119:282–290PubMedGoogle Scholar
  107. Lieber CS (2004) The discovery of the microsomal ethanol oxidizing system and its physiologic and pathologic role. Drug Metab Rev 36:511–529. doi: 10.1081/DMR-200033441 PubMedGoogle Scholar
  108. Lindtner C (2013) Binge drinking induces whole-body insulin resistance by impairing hypothalamic insulin action. Sci Transl Med 5:170ra114. doi: 10.1126/scitranslmed.3005123, PMCID: PMC3740748Google Scholar
  109. Liu X, Zha J, Nishitani J, Chen H, Zack JA (2003) HIV-1 infection in peripheral blood lymphocytes (PBLs) exposed to alcohol. Virology 307:37–44PubMedGoogle Scholar
  110. Loganantharaj N et al (2014) The effects of chronic binge alcohol on the genital microenvironment of simian immunodeficiency virus-infected female rhesus macaques. AIDS Res Hum Retrovir 30:783–791. doi: 10.1089/aid.2014.0065, PMCID: PMC4118703PubMedCentralPubMedGoogle Scholar
  111. Marcondes MC, Watry D, Zandonatti M, Flynn C, Taffe MA, Fox H (2008) Chronic alcohol consumption generates a vulnerable immune environment during early SIV infection in rhesus macaques. Alcohol Clin Exp Res 32:1583–1592. doi: 10.1111/j.1530-0277.2008.00730.x, PMCID: PMC2579901PubMedCentralPubMedGoogle Scholar
  112. Martin F, Ward K, Slavin G, Levi J, Peters TJ (1985) Alcoholic skeletal myopathy, a clinical and pathological study. Quart J Med 55:233–251PubMedGoogle Scholar
  113. Mastrogiannis DS et al (2014) Alcohol enhances HIV infection of cord blood monocyte-derived macrophages. Curr HIV Res 12:301–308, PMCID: PMC4153785PubMedCentralPubMedGoogle Scholar
  114. McClure HM, Anderson DC, Ansari AA, Fultz PN, Klumpp SA, Schinazi RF (1990) Nonhuman primate models for evaluation of AIDS therapy. Ann N Y Acad Sci 616:287–298PubMedGoogle Scholar
  115. Merroun I et al (2009) Influence of intracerebroventricular or intraperitoneal administration of cannabinoid receptor agonist (WIN 55,212-2) and inverse agonist (AM 251) on the regulation of food intake and hypothalamic serotonin levels. British J Nutri 101:1569–1578. doi: 10.1017/S0007114508083530 Google Scholar
  116. Meyerhoff DJ (2001) Effects of alcohol and HIV infection on the central nervous system. Alcohol Res Health : J Nat Instit Alcohol Abuse Alcoholism 25:288–298Google Scholar
  117. Miguez MJ, Shor-Posner G, Morales G, Rodriguez A, Burbano X (2003) HIV treatment in drug abusers: impact of alcohol use. Addict Biol 8:33–37. doi: 10.1080/1355621031000069855 PubMedGoogle Scholar
  118. Milloy MJ et al (2014) High-intensity cannabis use associated with lower plasma human immunodeficiency virus-1 RNA viral load among recently infected people who use injection drugs. Drug Alcohol Rev. doi: 10.1111/dar.12223 PubMedGoogle Scholar
  119. Mize AL, Alper RH (2000) Acute and long-term effects of 17beta-estradiol on G(i/o) coupled neurotransmitter receptor function in the female rat brain as assessed by agonist-stimulated [35S] GTPgammaS binding. Brain Res 859:326–333PubMedGoogle Scholar
  120. Mohri H, Bonhoeffer S, Monard S, Perelson AS, Ho DD (1998) Rapid turnover of T lymphocytes in SIV-infected rhesus macaques. Science (New York, NY) 279:1223–1227Google Scholar
  121. Molina PE et al (2006) Chronic alcohol accentuates nutritional, metabolic, and immune alterations during asymptomatic simian immunodeficiency virus infection. Alcohol Clin Exp Res 30:2065–2078. doi: 10.1111/j.1530-0277.2006.00252.x PubMedGoogle Scholar
  122. Molina PE, Lang CH, McNurlan M, Bagby GJ, Nelson S (2008) Chronic alcohol accentuates simian acquired immunodeficiency syndrom-associated wasting. Alcohol Clin Exp Res 32:138–147, PMCID: PMC3178106PubMedCentralPubMedGoogle Scholar
  123. Molina PE, Amedee A, LeCapitaine NJ, Zabaleta J, Mohan M, Winsauer P, Vande Stouwe C (2011a) Cannabinoid neuroimmune modulation of SIV disease. J Neuroimmune Pharmacol : Off J Soc NeuroImmune Pharmacol 6:516–527. doi: 10.1007/s11481-011-9301-8, PMCID: PMC3208744Google Scholar
  124. Molina PE et al (2011b) Cannabinoid administration attenuates the progression of simian immunodeficiency virus. AIDS Res Hum Retrovir 27:585–592. doi: 10.1089/AID.2010.0218, PMCID: PMC3131805PubMedCentralPubMedGoogle Scholar
  125. Molina PE et al (2014) Modulation of gut-specific mechanisms by chronic delta(9)-tetrahydrocannabinol administration in male rhesus macaques infected with simian immunodeficiency virus: a systems biology analysis. AIDS Res Hum Retrovir 30:567–578. doi: 10.1089/aid.2013.0182, PMCID: PMC4046212PubMedCentralPubMedGoogle Scholar
  126. Morahan PS, Klykken PC, Smith SH, Harris LS, Munson AE (1979) Effects of cannabinoids on host resistance to Listeria monocytogenes and herpes simplex virus. Infect Immun 23:670–674, PMCID: PMC414217PubMedCentralPubMedGoogle Scholar
  127. Muniyappa R et al (2013) Metabolic effects of chronic cannabis smoking. Diabetes Care 36:2415–2422. doi: 10.2337/dc12-2303, PMCID: PMC3714514PubMedCentralPubMedGoogle Scholar
  128. Murray EA, Rausch DM, Lendvay J, Sharer LR, Eiden LE (1992) Cognitive and motor impairments associated with SIV infection in rhesus monkeys. Science (New York, NY) 255:1246–1249Google Scholar
  129. Nair MP, Mahajan S, Hewitt R, Whitney ZR, Schwartz SA (2004) Association of drug abuse with inhibition of HIV-1 immune responses: studies with long-term of HIV-1 non-progressors. J Neuroimmunol 147:21–25PubMedGoogle Scholar
  130. Nelson S, Bagby GJ (2011) Alcohol and HIV infection. Trans Am Clin Climatol Assoc 122:244–253, PMCID: PMC3116369PubMedCentralPubMedGoogle Scholar
  131. Nelson S, Happel KI, Zhang P, Myers L, Dufour JP, Bagby GJ (2013) Effect of bacterial pneumonia on lung simian immunodeficiency virus (SIV) replication in alcohol consuming SIV-infected rhesus macaques Alcohol Clin Exp Res 37:969-977 doi:10.1111/acer.12070. PMCID: PMC3661707.Google Scholar
  132. Newman SP, Lunn S, Harrison MJ (1995) Do asymptomatic HIV-seropositive individuals show cognitive deficit? Aids 9:1211–1220PubMedGoogle Scholar
  133. Newton CA, Klein TW, Friedman H (1994) Secondary immunity to Legionella pneumophila and Th1 activity are suppressed by delta-9-tetrahydrocannabinol injection. Infect Immun 62:4015–4020, PMCID: PMC303061PubMedCentralPubMedGoogle Scholar
  134. Nguyen VA, Le T, Tong M, Silbermann E, Gundogan F, de la Monte SM (2012) Impaired insulin/IGF signaling in experimental alcohol-related myopathy. Nutrients 4:1058–1075. doi: 10.3390/nu4081058, PMCID: PMC3448087PubMedCentralPubMedGoogle Scholar
  135. Nicolas JM et al (2001) Increased circulating leptin levels in chronic alcoholism. Alcohol Clin Exp Res 25:83–88PubMedGoogle Scholar
  136. O’Sullivan SE (2007) Cannabinoids go nuclear: evidence for activation of peroxisome proliferator-activated receptors. Br J Pharmacol 152:576–582. doi: 10.1038/sj.bjp.0707423, PMCID: PMC2190029PubMedCentralPubMedGoogle Scholar
  137. Pahar B et al (2013) Effects of alcohol consumption on antigen-specific cellular and humoral immune responses to SIV in rhesus macaques. J Acquir Immune Defic Syndr 64:332–341. doi: 10.1097/QAI.0b013e31829f6dca, PMCID: PMC3812314PubMedGoogle Scholar
  138. Penner EA, Buettner H, Mittleman MA (2013) The impact of marijuana use on glucose, insulin, and insulin resistance among US adults. Am J Med 126:583–589. doi: 10.1016/j.amjmed.2013.03.002 PubMedGoogle Scholar
  139. Pertwee RG (2008) The diverse CB1 and CB2 receptor pharmacology of three plant cannabinoids: delta9-tetrahydrocannabinol, cannabidiol and delta9-tetrahydrocannabivarin. Br J Pharmacol 153:199–215. doi: 10.1038/sj.bjp.0707442, PMCID: PMC2219532PubMedCentralPubMedGoogle Scholar
  140. Pertwee RG, Stevenson LA, Griffin G (1993) Cross-tolerance between delta-9-tetrahydrocannabinol and the cannabimimetic agents, CP 55,940, WIN 55,212-2 and anandamide. Br J Pharmacol 110:1483–1490, PMCID: PMC2175863PubMedCentralPubMedGoogle Scholar
  141. Phillips SJ, Freedberg KA, Traphagen ET, Horton NJ, Samet JH (2001) Screening for alcohol problems in HIV-infected primary care patients. J Gen Int Med 16:165Google Scholar
  142. Poonia B, Nelson S, Bagby GJ, Veazey RS (2006a) Intestinal lymphocyte subsets and turnover are affected by chronic alcohol consumption: implications for SIV/HIV infection. J Acquir Immune Defic Syndr 41:537–547. doi: 10.1097/ PubMedGoogle Scholar
  143. Poonia B, Nelson S, Bagby GJ, Zhang P, Quniton L, Veazey RS (2006b) Chronic alcohol consumption results in higher simian immunodeficiency virus replication in mucosally inoculated rhesus macaques. AIDS Res Hum Retrovir 22:589–594. doi: 10.1089/aid.2006.22.589 PubMedGoogle Scholar
  144. Prospero-Garcia O, Gold LH, Fox HS, Polis I, Koob GF, Bloom FE, Henriksen SJ (1996) Microglia-passaged simian immunodeficiency virus induces neurophysiological abnormalities in monkeys. Proc Natl Acad Sci U S A 93:14158–14163, PMCID: PMC19510PubMedCentralPubMedGoogle Scholar
  145. Pross SH, Klein TW, Newton CA, Smith J, Widen R, Friedman H (1990) Differential suppression of T-cell subpopulations by thc (delta-9-tetrahydrocannabinol). Int J Immunopharmacol 12:539–544PubMedGoogle Scholar
  146. Purohit V, Gao B, Song BJ (2009) Molecular mechanisms of alcoholic fatty liver. Alcohol Clin Exp Res 33:191–205. doi: 10.1111/j.1530-0277.2008.00827.x, PMCID: PMC2633431PubMedCentralPubMedGoogle Scholar
  147. Raj A et al (2009) The associations of binge alcohol use with HIV/STI risk and diagnosis among heterosexual African American men. Drug Alcohol Depend 101:101–106. doi: 10.1016/j.drugalcdep.2008.11.008 PubMedGoogle Scholar
  148. Rajavashisth TB, Shaheen M, Norris KC, Pan D, Sinha SK, Ortega J, Friedman TC (2012) Decreased prevalence of diabetes in marijuana users: cross-sectional data from the National Health and Nutrition Examination Survey (NHANES) III. BMJ Open 2:e000494. doi: 10.1136/bmjopen-2011-000494, PMCID: PMC3289985PubMedCentralPubMedGoogle Scholar
  149. Ramirez SH et al (2013) Attenuation of HIV-1 replication in macrophages by cannabinoid receptor 2 agonists. J Leukoc Biol 93:801–810. doi: 10.1189/jlb.1012523, PMCID: PMC3629438PubMedCentralPubMedGoogle Scholar
  150. Rasouli N, Kern PA (2008) Adipocytokines and the metabolic complications of obesity. J Clin Endocrinol Metab 93:S64–S73. doi: 10.1210/jc.2008-1613, PMCID: PMC2585759PubMedCentralPubMedGoogle Scholar
  151. Rausch DM et al (1994) Cytopathologic and neurochemical correlates of progression to motor/cognitive impairment in SIV-infected rhesus monkeys. J Neuropathol Exp Neurol 53:165–175PubMedGoogle Scholar
  152. Raymond LA et al (1999) Motor evoked potentials in a rhesus macaque model of neuro-AIDS. J Neurovirol 5:217–231PubMedGoogle Scholar
  153. Riebe CJ, Hill MN, Lee TT, Hillard CJ, Gorzalka BB (2010) Estrogenic regulation of limbic cannabinoid receptor binding. Psychoneuroendocrinology 35:1265–1269. doi: 10.1016/j.psyneuen.2010.02.008, PMCID: PMC2933663PubMedCentralPubMedGoogle Scholar
  154. Rodger DA et al (2011) A study in HIV outpatients to assess prevalence of cognitive disorders, associated features and impact on risk behaviours. Cell Stress Chaperones 12:e1. doi: 10.1379/1466-1268(2007)12[e1:AFTRIC]2.0.CO;2 Google Scholar
  155. Rodriguez de Fonseca F, Cebeira M, Ramos JA, Martin M, Fernandez-Ruiz JJ (1994) Cannabinoid receptors in rat brain areas: sexual differences, fluctuations during estrous cycle and changes after gonadectomy and sex steroid replacement. Life Sci 54:159–170PubMedGoogle Scholar
  156. Rogers CQ, Ajmo JM, You M (2008) Adiponectin and alcoholic fatty liver disease. IUBMB life 60:790–797. doi: 10.1002/iub.124 PubMedGoogle Scholar
  157. Rom S, Persidsky Y (2013) Cannabinoid receptor 2: potential role in immunomodulation and neuroinflammation. J Neuroimmune Pharmacol : Off J Soc NeuroImmune Pharmacol 8:608–620. doi: 10.1007/s11481-013-9445-9, PMCID: PMC3663904Google Scholar
  158. Romero J (1998) Time-course of the cannabinoid receptor down-regulation in the adult rat brain caused by repeated exposure to delta9-tetrahydrocannabinol. Synapse (New York, NY) 30:298–308. doi: 10.1002/(sici)1098-2396(199811)30:3<298::aid-syn7>;2-6 Google Scholar
  159. Ronis MJ, Wands JR, Badger TM, de la Monte SM, Lang CH, Calissendorff J (2007) Alcohol-induced disruption of endocrine signaling. Alcohol Clin Exp Res 31:1269–1285. doi: 10.1111/j.1530-0277.2007.00436.x PubMedGoogle Scholar
  160. Rothlind JC, Greenfield TM, Bruce AV, Meyerhoff DJ, Flenniken DL, Lindgren JA, Weiner MW (2005) Heavy alcohol consumption in individuals with HIV infection: effects on neuropsychological performance. J Int Neuropsychol Soc : JINS 11:70–83. doi: 10.1017/s1355617705050095, PMCID: PMC2376753PubMedCentralPubMedGoogle Scholar
  161. SAMSHA SAaMHSA (2005) Results from the 2004 National survey on druge use and health: National Findings. vol NSDUH Series H-36. Rockville, MDGoogle Scholar
  162. SAMHSA (2004) Overview of findings from the 2003 National Survey on Drug Use and Health vol Office of Applied Studies, NSDUH Series H-24, DHHS Publication No. SMA 04-3963. Rockville, MDGoogle Scholar
  163. SAMHSA SAaMHSA (2009) Treatment episode data set (TEDS) series vol U.S. Department of Health and Human Services, Ann ArborGoogle Scholar
  164. Sandler NG et al (2014) Type I interferon responses in rhesus macaques prevent SIV infection and slow disease progression. Nature 511:601–605. doi: 10.1038/nature13554 PubMedCentralPubMedGoogle Scholar
  165. Sassoon SA, Fama R, Rosenbloom MJ, O’Reilly A, Pfefferbaum A, Sullivan EV (2007) Component cognitive and motor processes of the digit symbol test: differential deficits in alcoholism, HIV infection, and their comorbidity. Alcohol Clin Exp Res 31:1315–1324. doi: 10.1111/j.1530-0277.2007.00426.x PubMedGoogle Scholar
  166. Sevastianova K, Sutinen J, Kannisto K, Hamsten A, Ristola M, Yki-Jarvinen H (2008) Adipose tissue inflammation and liver fat in patients with highly active antiretroviral therapy-associated lipodystrophy. Am J Physiol Endocrinol Metab 295:E85–E91. doi: 10.1152/ajpendo.90224.2008 PubMedGoogle Scholar
  167. Shay AH et al (2003) Impairment of antimicrobial activity and nitric oxide production in alveolar macrophages from smokers of marijuana and cocaine. J Infect Dis 187:700–704. doi: 10.1086/368370 PubMedGoogle Scholar
  168. Shuper PA, Joharchi N, Irving H, Rehm J (2009) Alcohol as a correlate of unprotected sexual behavior among people living with HIV/AIDS: review and meta-analysis. AIDS Behav 13:1021–1036. doi: 10.1007/s10461-009-9589-z PubMedGoogle Scholar
  169. Simon L et al (2014) Chronic binge alcohol consumption alters myogenic gene expression and reduces in vitro myogenic differentiation potential of myoblasts from rhesus macaques. Am J Physiol Regulat, Integrat Compara Physiol 306:R837–R844. doi: 10.1152/ajpregu.00502.2013, PMCID: PMC4042206Google Scholar
  170. Sim-Selley LJ (2003) Regulation of cannabinoid CB1 receptors in the central nervous system by chronic cannabinoids. Crit Rev Neurobiol 15:91–119PubMedGoogle Scholar
  171. Slawson G et al (2014) High-intensity cannabis use and adherence to antiretroviral therapy among people who use illicit drugs in a Canadian setting. AIDS Behav. doi: 10.1007/s10461-014-0847-3 Google Scholar
  172. Smit E, Crespo CJ (2001) Dietary intake and nutritional status of US adult marijuana users: results from the third national health and nutrition examination survey. Public Health Nutr 4:781–786PubMedGoogle Scholar
  173. Snider WD, Simpson DM, Nielsen S, Gold JW, Metroka CE, Posner JB (1983) Neurological complications of acquired immune deficiency syndrome: analysis of 50 patients. Ann Neurol 14:403–418. doi: 10.1002/ana.410140404 PubMedGoogle Scholar
  174. Specter S, Lancz G, Westrich G, Friedman H (1991) Delta-9-tetrahydrocannabinol augments murine retroviral induced immunosuppression and infection. Int J Immunopharmacol 13:411–417PubMedGoogle Scholar
  175. Struwe M et al (1993) Effect of dronabinol on nutritional status in HIV infection. Ann Pharmacother 27:827–831PubMedGoogle Scholar
  176. Teixeira D, Pestana D, Faria A, Calhau C, Azevedo I, Monteiro R (2010) Modulation of adipocyte biology by delta(9)-tetrahydrocannabinol. Obesity (Silver Spring) 18:2077–2085. doi: 10.1038/oby.2010.100 Google Scholar
  177. The NSDUH Report: Substance use and mental health estimates from the 2013 National Survey on Drug Use and Health: Overview of Findings (2014). Rockville, MDGoogle Scholar
  178. Theall KP, Amedee A, Clark RA, Dumestre J, Kissinger P (2008) Alcohol consumption and HIV-1 vaginal RNA shedding among women. J Stud Alcohol Drugs 69:454–458PubMedGoogle Scholar
  179. Tindall B, Cooper DA, Donovan B, Barnes T, Philpot CR, Gold J, Penny R (1988) The Sydney AIDS Project: development of acquired immunodeficiency syndrome in a group of HIV seropositive homosexual men. Aust NZ J Med 18:8–15Google Scholar
  180. Villares J (2007) Chronic use of marijuana decreases cannabinoid receptor binding and mRNA expression in the human brain. Neuroscience 145:323–334. doi: 10.1016/j.neuroscience.2006.11.012 PubMedGoogle Scholar
  181. Weiss L, Zeira M, Reich S, Har-Noy M, Mechoulam R, Slavin S, Gallily R (2006) Cannabidiol lowers incidence of diabetes in non-obese diabetic mice. Autoimmunity 39:143–151. doi: 10.1080/08916930500356674 PubMedGoogle Scholar
  182. Wilson WH, Ellinwood EH, Mathew RJ, Johnson K (1994) Effects of marijuana on performance of a computerized cognitive-neuromotor test battery. Psychiatry Res 51:115–125PubMedGoogle Scholar
  183. Winsauer PJ, Moerschbaecher JM, Brauner IN, Purcell JE, Lancaster JR Jr, Bagby GJ, Nelson S (2002) Alcohol unmasks simian immunodeficiency virus-induced cognitive impairments in rhesus monkeys. Alcohol Clin Exp Res 26:1846–1857. doi: 10.1097/01.alc.0000042171.80435.f1 PubMedGoogle Scholar
  184. Winsauer PJ et al (2011a) Long-term behavioral and pharmacodynamic effects of delta-9-tetrahydrocannabinol in female rats depend on ovarian hormone status. Addict Biol 16:64–81, PMCID: PMC3057667PubMedCentralPubMedGoogle Scholar
  185. Winsauer PJ et al (2011b) Tolerance to chronic delta-9-tetrahydrocannabinol (Delta(9)-THC) in rhesus macaques infected with simian immunodeficiency virus. Exp Clin Psychopharmacol 19:154–172. doi: 10.1037/a0023000, PMCID: PMC3140653PubMedCentralPubMedGoogle Scholar
  186. Woolridge E, Barton S, Samuel J, Osorio J, Dougherty A, Holdcroft A (2005) Cannabis use in HIV for pain and other medical symptoms. J Pain Symptom Manag 29:358–367. doi: 10.1016/j.jpainsymman.2004.07.011 Google Scholar
  187. Yki-Jarvinen H, Nikkila EA (1985) Ethanol decreases glucose utilization in healthy man. J Clin Endocrinol Metabol 61:941–945Google Scholar
  188. You M, Rogers CQ (2009) Adiponectin: a key adipokine in alcoholic fatty liver. Exp Biol Med (Maywood) 234:850–859. doi: 10.3181/0902-MR-61 Google Scholar
  189. You M, Considine RV, Leone TC, Kelly DP, Crabb DW (2005) Role of adiponectin in the protective action of dietary saturated fat against alcoholic fatty liver in mice. Hepatology 42:568–577. doi: 10.1002/hep.20821, PMCID: PMC1398076PubMedCentralPubMedGoogle Scholar
  190. Yuan M, Kiertscher SM, Cheng Q, Zoumalan R, Tashkin DP, Roth MD (2002) Delta 9-Tetrahydrocannabinol regulates Th1/Th2 cytokine balance in activated human T cells. J Neuroimmunol 133:124–131PubMedGoogle Scholar
  191. Zhu W, Friedman H, Klein TW (1998) Delta9-tetrahydrocannabinol induces apoptosis in macrophages and lymphocytes: involvement of Bcl-2 and caspase-1. J Pharmacol Experiment Therapeut 286:1103–1109Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Patricia E. Molina
    • 1
    • 4
    Email author
  • Angela M. Amedee
    • 2
    • 4
  • Peter Winsauer
    • 3
    • 4
  • Steve Nelson
    • 4
  • Gregory Bagby
    • 1
    • 4
  • Liz Simon
    • 1
    • 4
  1. 1.Department of PhysiologyLouisiana State University Health Sciences Center, School of MedicineNew OrleansUSA
  2. 2.Department of Microbiology, Immunology, & ParasitologyLouisiana State University Health Sciences Center, School of MedicineNew OrleansUSA
  3. 3.Department of PharmacologyLouisiana State University Health Sciences Center, School of MedicineNew OrleansUSA
  4. 4.Alcohol and Drug Abuse Center of ExcellenceLouisiana State University Health Sciences Center, School of MedicineNew OrleansUSA

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