Abstract
Globally, cannabis is the most commonly used illicit drug, with disproportionately high use among persons with HIV. Despite advances in HIV care, nearly half of persons living with HIV continue to experience neurocognitive deficits or impairments that may have negative impacts on their daily function. Chronic cannabis use may play a role in the development or exacerbation of these impairments. Here we present a review summarizing existing research detailing the effect of cannabis use associated with the neuropathogenesis of HIV. We examine evidence for possible additive or synergistic effects of HIV infection and cannabis use on neuroHIV in both the preclinical and adult human literatures, including in vitro studies, animal models, clinical neuroimaging research, and studies examining the cognitive effects of cannabis. We discuss the limitations of existing research, including methodological challenges involved with clinical research with human subjects. We identify gaps in the field and propose critical research questions to advance our understanding of how cannabis use affects neuroHIV.
Graphical Abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abrams DI et al (2007) Cannabis in painful HIV-associated sensory neuropathy: a randomized placebo-controlled trial. Neurology 68:515–521. https://doi.org/10.1212/01.wnl.0000253187.66183.9c
Aizpurua-Olaizola O et al (2016) Evolution of the cannabinoid and terpene content during the growth of Cannabis sativa plants from different chemotypes. J Nat Prod 79:324–331. https://doi.org/10.1021/acs.jnatprod.5b00949
Ances BM, Hammoud DA (2014) Neuroimaging of HIV associated neurocognitive disorders (HAND). Curr Opin HIV AIDS 9:545
Araque A, Castillo PE, Manzoni OJ, Tonini R (2017) Synaptic functions of endocannabinoid signaling in health and disease. Neuropharmacology 124:13–24. https://doi.org/10.1016/j.neuropharm.2017.06.017
Arnone D, Barrick TR, Chengappa S, Mackay CE, Clark CA, Abou-Saleh MT (2008) Corpus callosum damage in heavy marijuana use: preliminary evidence from diffusion tensor tractography and tract-based spatial statistics. Neuroimage 41:1067–1074. https://doi.org/10.1016/j.neuroimage.2008.02.064
Atwood BK, Mackie K (2010) CB2: a cannabinoid receptor with an identity crisis. Br J Pharmacol 160:467–479. https://doi.org/10.1111/j.1476-5381.2010.00729.x
Avraham HK et al (2015) Impaired neurogenesis by HIV-1-Gp120 is rescued by genetic deletion of fatty acid amide hydrolase enzyme. Br J Clin Pharmacol 172:4603–4614. https://doi.org/10.1111/bph.12657
Avraham HK et al (2014) The cannabinoid CB(2) receptor agonist AM1241 enhances neurogenesis in GFAP/Gp120 transgenic mice displaying deficits in neurogenesis. Br J Clin Pharmacol 171:468–479. https://doi.org/10.1111/bph.12478
Becker MP, Collins PF, Lim KO, Muetzel RL, Luciana M (2015) Longitudinal changes in white matter microstructure after heavy cannabis use. Dev Cogn Neurosci 16:23–35. https://doi.org/10.1016/j.dcn.2015.10.004
Benamar K1, Yondorf M, Geller EB, Eisenstein TK, Adler MW. (2009) Physiological evidence for interaction between the HIV-1 co-receptor CXCR4 and the cannabinoid system in the brain. Br J Pharmacol. 157(7):1225-31. doi: 10.1111/j.1476-5381.2009.00285.x. Epub 2009 Jun 22.
Benito C et al (2005) A glial endogenous cannabinoid system is upregulated in the brains of macaques with simian immunodeficiency virus-induced encephalitis. J Neurosci 25:2530–2536. https://doi.org/10.1523/JNEUROSCI.3923-04.2005
Blest-Hopley G, O'Neill A, Wilson R, Giampietro V, Lythgoe D, Egerton A, Bhattacharyya S (2019) Adolescent-onset heavy cannabis use associated with significantly reduced glial but not neuronal markers and glutamate levels in the hippocampus. Addict Biol:[Epub ahead of print] doi:https://doi.org/10.1111/adb.12827
Broyd SJ, van Hell HH, Beale C, Yucel M, Solowij N (2016) Acute and chronic effects of cannabinoids on human cognition—a systematic review. Biol Psychiatry 79:557–567. https://doi.org/10.1016/j.biopsych.2015.12.002
Brumback T, Castro N, Jacobus J, Tapert S (2016) Effects of marijuana use on brain structure and function: neuroimaging findings from a neurodevelopmental perspective. Int Rev Neurobiol 129:33–65. https://doi.org/10.1016/bs.irn.2016.06.004
Buckley RF et al (2017) Functional network integrity presages cognitive decline in preclinical Alzheimer disease. Neurology 89:29–37. https://doi.org/10.1212/wnl.0000000000004059
Byrd DA et al (2011) Neurocognitive impact of substance use in HIV infection. J Acquir Immune Defic Syndr 58:154–162. https://doi.org/10.1097/QAI.0b013e318229ba41
Cabral GA, Griffin-Thomas L (2009) Emerging role of the cannabinoid receptor CB2 in immune regulation: therapeutic prospects for neuroinflammation. Expert Rev Mol Med 11:e3. https://doi.org/10.1017/s1462399409000957
Cabral GA, Jamerson M (2014) Marijuana use and brain immune mechanisms. Int Rev Neurobiol 118:199–230. https://doi.org/10.1016/b978-0-12-801284-0.00008-7
Cattie JE, Doyle K, Weber E, Grant I, Woods SP (2012) Planning deficits in HIV-associated neurocognitive disorders: component processes, cognitive correlates, and implications for everyday functioning. J Clin Exp Neuropsychol 34:906–918. https://doi.org/10.1080/13803395.2012.692772
Center for Behavioral Health Statistics and Quality (2015) Treatment Episode Data Set (TEDS): 2003–2013. National Admissions to Substance Abuse Treatment Services
Chang L, Chronicle EP (2007) Functional imaging studies in cannabis users. Neuroscientist 13:422–432. https://doi.org/10.1177/1073858406296601
Chang L, Cloak C, Yakupov R, Ernst T (2006a) Combined and independent effects of chronic marijuana use and HIV on brain metabolites. J Neuroimmune Pharmacol 1:65–76. https://doi.org/10.1007/s11481-005-9005-z
Chang L, Shukla DK (2018) Imaging studies of the HIV-infected brain. In: Brew BJ (ed) Handbook of Clinical Neurology, vol 152. Elsevier, Oxford, pp 229–264. https://doi.org/10.1016/B978-0-444-63849-6.00018-9
Chang L, Yakupov R, Cloak C, Ernst T (2006b) Marijuana use is associated with a reorganized visual-attention network and cerebellar hypoactivation. Brain 129:1096–1112. https://doi.org/10.1093/brain/awl064
Colizzi M, McGuire P, Pertwee RG, Bhattacharyya S (2016) Effect of cannabis on glutamate signalling in the brain: a systematic review of human and animal evidence. Neurosci Biobehav Rev 64:359–381. https://doi.org/10.1016/j.neubiorev.2016.03.010
Contreras JA, Goni J, Risacher SL, Sporns O, Saykin AJ (2015) The structural and functional connectome and prediction of risk for cognitive impairment in older adults. Curr Behav Neurosci Rep 2:234–245. https://doi.org/10.1007/s40473-015-0056-z
Copeland J, Pokorski I (2016) Progress toward pharmacotherapies for cannabis-use disorder: an evidence-based review. Subst Abuse Rehabil 7:41–53 doi:https://doi.org/10.2147/sar.s89857
Crane HM et al (2017) Prevalence and factors associated with hazardous alcohol use among persons living with HIV across the US in the current era of antiretroviral treatment. AIDS Behav 21:1914–1925. https://doi.org/10.1007/s10461-017-1740-7
Crane NA, Schuster RM, Fusar-Poli P, Gonzalez R (2013) Effects of cannabis on neurocognitive functioning: Recent advances, neurodevelopmental influences, and sex differences. Neuropsychol Rev 23:117–137. https://doi.org/10.1007/s11065-012-9222-1
Crean RD, Crane NA, Mason BJ (2011) An evidence-based review of acute and long-term effects of cannabis use on executive cognitive functions. J Addict Med 5:1–8
Cristiani SA, Pukay-Martin ND, Bornstein RA (2004) Marijuana use and cognitive function in HIV-infected people. J Neuropsychiatry Clin Neurosci 16:330–335
D'Souza G et al (2012) Medicinal and recreational marijuana use among HIV-infected women in the Women's Interagency HIV Cohort (WIHS), 1994–2010. J Acquir Immune Defic Syndr 61:618–626. https://doi.org/10.1097/QAI.0b013e318273ab3a
Dager AD et al (2018) Relationship between fMRI response during a nonverbal memory task and marijuana use in college students. Drug Alcohol Depend 188:71–78
De Petrocellis L, Di Marzo V (2009) An introduction to the endocannabinoid system: from the early to the latest concepts. Best Pract Res Clin Endocrinol Metab 23:1–15. https://doi.org/10.1016/j.beem.2008.10.013
Elliott DM, Singh N, Nagarkatti M, Nagarkatti PS (2018) Cannabidiol attenuates experimental autoimmune encephalomyelitis model of multiple sclerosis through induction of myeloid-derived suppressor cells. Front Immunol 9:1782. https://doi.org/10.3389/fimmu.2018.01782
Ernst T, Jiang CS, Nakama H, Buchthal S, Chang L (2010) Lower brain glutamate is associated with cognitive deficits in HIV patients: a new mechanism for HIV-associated neurocognitive disorder. J Magn Reson Imaging 32:1045–1053. https://doi.org/10.1002/jmri.22366
Esposito G et al (2002) The endocannabinoid system protects rat glioma cells against HIV-1 Tat protein-induced cytotoxicity. Mechanism and regulation J Biol Chem 277:50348–50354. https://doi.org/10.1074/jbc.M207170200
Esposito G et al (2011) Cannabidiol reduces Abeta-induced neuroinflammation and promotes hippocampal neurogenesis through PPARgamma involvement. PLoS One 6:e28668. https://doi.org/10.1371/journal.pone.0028668
Filbey FM, Aslan S, Calhoun VD, Spence JS, Damaraju E, Caprihan A, Segall J (2014) Long-term effects of marijuana use on the brain. Proc Natl Acad Sci U S A 111:16913–16918. https://doi.org/10.1073/pnas.1415297111
Fogarty A, Rawstorne P, Prestage G, Crawford J, Grierson J, Kippax S (2007) Marijuana as therapy for people living with HIV/AIDS: social and health aspects. AIDS Care 19:295–301. https://doi.org/10.1080/09540120600841930
Fraga D, Raborn ES, Ferreira GA, Cabral GA (2011) Cannabinoids inhibit migration of microglial-like cells to the HIV protein Tat. J Neuroimmune Pharmacol 6:566–577. https://doi.org/10.1007/s11481-011-9291-6
Freeman TP, Winstock AR (2015) Examining the profile of high-potency cannabis and its association with severity of cannabis dependence. Psychol Med 45:3181–3189. https://doi.org/10.1017/s0033291715001178
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. https://doi.org/10.1089/108729104323038892
Gamarel KE, Brown L, Kahler CW, Fernandez MI, Bruce D, Nichols S (2016) Prevalence and correlates of substance use among youth living with HIV in clinical settings. Drug Alcohol Depend 169:11–18. https://doi.org/10.1016/j.drugalcdep.2016.10.002
Gates TM, Cysique LA (2016) The chronicity of HIV infection should drive the research strategy of neuroHIV treatment studies: a critical review. CNS Drugs 30:53–69. https://doi.org/10.1007/s40263-015-0302-7
Gonzalez R, Schuster RM, Vassileva J, Martin EM (2011) Impact of HIV and a history of marijuana dependence on procedural learning among individuals with a history of substance dependence. J Clin Exp Neuropsychol 33:735–752. https://doi.org/10.1080/13803395.2011.553584
Gorantla S1, Makarov E, Roy D, Finke-Dwyer J, Murrin LC, Gendelman HE, Poluektova L. (2010) Immunoregulation of a CB2 receptor agonist in a murine model of neuroAIDS. J Neuroimmune Pharmacol. 5(3):456-68. https://doi.org/10.1007/s11481-010-9225. Epub 2010 Jun 12.
Grant I, Gonzalez R, Carey C, Natarajan L, Woflson T (2003) Non-acute (residual) neurocognitive effects of cannabis use: a meta-analytic study. J Int Neuropsychol Soc 9:679–689. https://doi.org/10.1017/S1355617703950016
Gruber SA, Silveri MM, Dahlgren MK, Yurgelun-Todd D (2011) Why so impulsive? White matter alterations are associated with impulsivity in chronic marijuana smokers. Exp Clin Psychopharmacol 19:231–242. https://doi.org/10.1037/a0023034
Haney M, Gunderson EW, Rabkin J, Hart CL, Vosburg SK, Comer SD, Foltin RW (2007) Dronabinol and marijuana in HIV(+) marijuana smokers: caloric intake, mood, and sleep. J Acquir Immune Defic Syndr 45:545–554. https://doi.org/10.1097/QAI.0b013e31811ed205
Haney M, Rabkin J, Gunderson E, Foltin RW (2005) Dronabinol and marijuana in HIV(+) marijuana smokers: acute effects on caloric intake and mood. Psychopharmacology 181:170–178. https://doi.org/10.1007/s00213-005-2242-2
Hartzler B et al (2017) Identifying HIV care enrollees at-risk for cannabis use disorder. AIDS Care 29:846–850. https://doi.org/10.1080/09540121.2016.1271393
Heaton RK et al (2010) HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology 75:2087–2096. https://doi.org/10.1212/WNL.0b013e318200d727
Heaton RK et al (2004) The impact of HIV-associated neuropsychological impairment on everyday functioning. J Int Neuropsychol Soc 10:317–331. https://doi.org/10.1017/S1355617704102130
Hellem T, Shi X, Latendresse G, Renshaw PF (2015) The utility of magnetic resonance spectroscopy for understanding substance use disorders: a systematic review of the literature. J Am Psychiatr Nurses Assoc 21:244–275. https://doi.org/10.1177/1078390315598606
Hermes DJ et al (2018) Neuroprotective effects of fatty acid amide hydrolase catabolic enzyme inhibition in a HIV-1 Tat model of neuroAIDS. Neuropharmacology 141:55–65. https://doi.org/10.1016/j.neuropharm.2018.08.013
Katz PS, Edwards S, Molina PE (2014) Cannabinoids. Springer, New York. https://doi.org/10.1007/978-1-4939-1071-7_23
Kennedy CA, Zerbo E (2014) HIV-related neurocognitive disorders and drugs of abuse: mired in confound, surrounded by risk. Curr Addict Rep 1:229–236. https://doi.org/10.1007/s40429-014-0028-5
Laverick R et al (2017) Self-reported decline in everyday function, cognitive symptoms, and cognitive function in people with HIV. J Acquir Immune Defic Syndr 76:e74–e83. https://doi.org/10.1097/qai.0000000000001468
Levine A, Ross J, González R, Martin E (2015) Neurocognitive functioning in HIV-infected substance users. In: Hope TJ, Richman D, Stevenson M (eds) Encyclopedia of AIDS. Springer, New York, pp 1–8. https://doi.org/10.1007/978-1-4614-9610-6_296-1
Lorkiewicz SA et al (2018) Lifetime marijuana and alcohol use, and cognitive dysfunction in people with human immunodeficiency virus infection. Subst Abus 39:116–123. https://doi.org/10.1080/08897077.2017.1391925
Maccarrone M et al (2004) Enhanced anandamide degradation is associated with neuronal apoptosis induced by the HIV-1 coat glycoprotein gp120 in the rat neocortex. J Neurochem 89:1293–1300. https://doi.org/10.1111/j.1471-4159.2004.02430.x
Mackie K (2005) Distribution of cannabinoid receptors in the central and peripheral nervous system Handb Exp Pharmacol 168:299–325
Manza P, Tomasi D, Volkow ND (2018) Subcortical local functional hyperconnectivity in Cannabis dependence. Biol Psychiatry Cogn Neurosci Neuroimaging 3:285–293. https://doi.org/10.1016/j.bpsc.2017.11.004
Mashhoon Y, Jensen JE, Sneider JT, Yurgelun-Todd DA, Silveri MM (2013) Lower left thalamic myo-inositol levels associated with greater cognitive impulsivity in marijuana-dependent young men: preliminary spectroscopic evidence at 4T. J Addict Res Ther Suppl 4 doi:https://doi.org/10.4172/2155-6105.s4-009
Meade CS, Bell RP, Towe SL, Chen NK, Hobkirk AL, Huettel SA (2018) Synergistic effects of marijuana abuse and HIV infection on neural activation during a cognitive interference task. Addict Biol 24:1235–1244. https://doi.org/10.1111/adb.12678
Mechoulam R, Parker LA (2013) The endocannabinoid system and the brain. Annu Rev Psychol 64:21–47. https://doi.org/10.1146/annurev-psych-113011-143739
Mehmedic Z et al (2010) Potency trends of Delta9-THC and other cannabinoids in confiscated cannabis preparations from 1993 to 2008. J Forensic Sci 55:1209–1217. https://doi.org/10.1111/j.1556-4029.2010.01441.x
Meier MH et al (2012) Persistent cannabis users show neuropsychological decline from childhood to midlife. Proc Natl Acad Sci U S A 109:E2657–E2664. https://doi.org/10.1073/pnas.1206820109
Mimiaga MJ et al (2013) Substance use among HIV-infected patients engaged in primary care in the United States: findings from the Centers for AIDS Research Network of Integrated Clinical Systems cohort. Am J Public Health 103:1457–1467. https://doi.org/10.2105/ajph.2012.301162
Nader DA, Sanchez ZM (2018) Effects of regular cannabis use on neurocognition, brain structure, and function: a systematic review of findings in adults. Am J Drug Alcohol Abuse 44:4–18. https://doi.org/10.1080/00952990.2017.1306746
National Conference of State Legislatures (2019) State Medical Marijuana Laws. http://www.ncsl.org/research/health/state-medical-marijuana-laws.
Okafor CN et al (2017a) Trajectories of marijuana use among HIV-seropositive and HIV-seronegative MSM in the Multicenter AIDS Cohort Study (MACS), 1984–2013. AIDS Behav 21:1091–1104. https://doi.org/10.1007/s10461-016-1445-3
Okafor CN et al (2017b) Marijuana use and viral suppression in persons receiving medical care for HIV-infection. Am J Drug Alcohol Abuse 43:103–110. https://doi.org/10.1080/00952990.2016.1191505
Pacula RL, Jacobson M, Maksabedian EJ (2016) In the weeds: a baseline view of cannabis use among legalizing states and their neighbours. Addiction 111:973–980. https://doi.org/10.1111/add.13282
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. https://doi.org/10.1038/sj.bjp.0707442
Prentiss D, Power R, Balmas G, Tzuang G, Israelski DM (2004) Patterns of marijuana use among patients with HIV/AIDS followed in a public health care setting. J Acquir Immune Defic Syndr 35:38–45. https://doi.org/10.1097/00126334-200401010-00005
Roth MD, Tashkin DP, Whittaker KM, Choi R, Baldwin GC (2005) Tetrahydrocannabinol suppresses immune function and enhances HIV replication in the huPBL-SCID mouse. Life Sci 77:1711–1722. https://doi.org/10.1016/j.lfs.2005.05.014
Saylor D et al (2016) HIV-associated neurocognitive disorder - pathogenesis and prospects for treatment. Nat Rev Neurol 12:309. https://doi.org/10.1038/nrneurol.2016.53
Schreiner AM, Dunn ME (2012) Residual effects of cannabis use on neurocognitive performance after prolonged abstinence: a meta-analysis. Exp Clin Psychopharmacol 20:420–429. https://doi.org/10.1037/a0029117
Silveri MM, Jensen JE, Rosso IM, Sneider JT, Yurgelun-Todd DA (2011) Preliminary evidence for white matter metabolite differences in marijuana-dependent young men using 2D J-resolved magnetic resonance spectroscopic imaging at 4 Tesla. Psychiatry Res 191:201–211. https://doi.org/10.1016/j.pscychresns.2010.10.005
Simon L et al (2016) Delta9-tetrahydrocannabinol (Delta9-THC) promotes neuroimmune-modulatory microRNA profile in striatum of Simian Immunodeficiency Virus (SIV)-infected macaques. J Neuroimmune Pharmacol 11:192–213. https://doi.org/10.1007/s11481-015-9645-6
Skalski LM, Towe SL, Sikkema KJ, Meade CS (2016) The impact of marijuana use on memory in HIV-infected patients: a comprehensive review of the HIV and marijuana literatures. Curr Drug Abuse Rev 9:126–141
Skalski LM, Towe SL, Sikkema KJ, Meade CS (2018) Memory impairment in HIV-infected individuals with early and late initiation of regular marijuana use. AIDS Behav 22:1596–1605. https://doi.org/10.1007/s10461-017-1898-z
Smith CD, Chebrolu H, Wekstein DR, Schmitt FA, Jicha GA, Cooper G, Markesbery WR (2007) Brain structural alterations before mild cognitive impairment. Neurology 68:1268–1273. https://doi.org/10.1212/01.wnl.0000259542.54830.34
Sneider JT, Mashhoon Y, Silveri MM (2013) A review of magnetic resonance spectroscopy studies in marijuana using adolescents and adults. J Addict Res Ther Suppl 4. https://doi.org/10.4172/2155-6105.s4-010
Solowij N, Battisti R (2008) The chronic effects of cannabis on memory in humans: a review. Curr Drug Abuse Rev 1:81–98. https://doi.org/10.2174/1874473710801010081
Srivastava MD, Srivastava BI, Brouhard B (1998) Delta9 tetrahydrocannabinol and cannabidiol alter cytokine production by human immune cells. Immunopharmacology 40:179–185. https://doi.org/10.1016/s0162-3109(98)00041-1
Tait R, Mackinnon A, Christensen H (2011) Cannabis use and cognitive function: 8-year trajectory in a young adult cohort. Addiction 106:2195–2203. https://doi.org/10.1111/j.1360-0443.2011.03574.x
Thames AD, Arentoft A, Rivera-Mindt M, Hinkin CH (2013) Functional disability in medication management and driving among individuals with HIV: a 1-year follow-up study. J Clin Exp Neuropsychol 35:49–58. https://doi.org/10.1080/13803395.2012.747596
Thames AD, Kuhn TP, Williamson TJ, Jones JD, Mahmood Z, Hammond A (2017) Marijuana effects on changes in brain structure and cognitive function among HIV(+) and HIV- adults. Drug Alcohol Depend 170:120–127. https://doi.org/10.1016/j.drugalcdep.2016.11.007
Thames AD, Mahmood Z, Burggren AC, Karimian A, Kuhn TP (2016) Combined effects of HIV and marijuana use on neurocognitive functioning and immune status. AIDS care 28:628–632. https://doi.org/10.1080/09540121.2015.1124983
Thomas B, ElSohy M (2016) The botany of Cannabis sativa L. Elsevier/RTI Press, Cambridge. https://doi.org/10.1016/C2014-0-03861-0
Towe SL, Horton OE, Martin B, Meade CS (2018) A comparison of motivations for marijuana use in HIV(+) and HIV(−) adults AIDS Behav 22:2807–2814. https://doi.org/10.1007/s10461-018-2123-4
United Nations (2018) Global overview of drug demand and supply: latest trends, cross-cutting issues. United Nations Office on Drugs and Crime, Vienna, Austria
Volkow ND, Baler RD, Compton WM, Weiss SR (2014) Adverse health effects of marijuana use. N Engl J Med 370:2219–2227. https://doi.org/10.1056/NEJMra1402309
Winsauer PJ et al (2011) Tolerance to chronic delta-9-tetrahydrocannabinol (Delta(9)-THC) in rhesus macaques infected with simian immunodeficiency virus. Exp Clin Psychopharmacol 19:154–172. https://doi.org/10.1037/a0023000
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 Manage 29:358–367. https://doi.org/10.1016/j.jpainsymman.2004.07.011
Xu C et al (2017) Endocannabinoids exert CB1 receptor-mediated neuroprotective effects in models of neuronal damage induced by HIV-1 Tat protein. Mol Cell Neurosci 83:92–102. https://doi.org/10.1016/j.mcn.2017.07.003
Zalesky A et al (2012) Effect of long-term cannabis use on axonal fibre connectivity. Brain 135:2245–2255. https://doi.org/10.1093/brain/aws136
Zhang X, Thayer SA (2018) Monoacylglycerol lipase inhibitor JZL184 prevents HIV-1 gp120-induced synapse loss by altering endocannabinoid signaling. Neuropharmacology 128:269–281. https://doi.org/10.1016/j.neuropharm.2017.10.023
Funding
This work was supported by grants from the United States National Institutes of Health (R01-DA045565 for SLT, CSM and RPB; R01-DA 035659 for CCC, JB and LC). The NIH had no further role in study design, data collection, analysis and interpretation of data, or the writing the report.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Towe, S.L., Meade, C.S., Cloak, C.C. et al. Reciprocal Influences of HIV and Cannabinoids on the Brain and Cognitive Function. J Neuroimmune Pharmacol 15, 765–779 (2020). https://doi.org/10.1007/s11481-020-09921-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11481-020-09921-y