Skip to main content

Advertisement

SpringerLink
Log in

Δ9-Tetrahydrocannabinol Treatment During Human Monocyte Differentiation Reduces Macrophage Susceptibility to HIV-1 Infection

  • ORIGINAL ARTICLE
  • Published:
Journal of Neuroimmune Pharmacology Aims and scope Submit manuscript

Abstract

The major psychoactive component of marijuana, Δ9-tetrahydrocannabinol (THC), also acts to suppress inflammatory responses. Receptors for THC, CB1, CB2, and GPR55, are differentially expressed on multiple cell types including monocytes and macrophages, which are important modulators of inflammation in vivo and target cells for HIV-1 infection. Use of recreational and medicinal marijuana is increasing, but the consequences of marijuana exposure on HIV-1 infection are unclear. Ex vivo studies were designed to investigate effects on HIV-1 infection in macrophages exposed to THC during or following differentiation. THC treatment of primary human monocytes during differentiation reduced HIV-1 infection of subsequent macrophages by replication competent or single cycle CCR5 using viruses. In contrast, treatment of macrophages with THC immediately prior to or continuously following HIV-1 exposure failed to alter infection. Specific receptor agonists indicated that the THC effect during monocyte differentiation was mediated primarily through CB2. THC reduced the number of p24 positive cells with little to no effect on virus production per infected cell, while quantitation of intracellular viral gag pinpointed the THC effect to an early event in the viral life cycle. Cells treated during differentiation with THC displayed reduced expression of CD14, CD16, and CD163 and donor dependent increases in mRNA expression of selected viral restriction factors, suggesting a fundamental alteration in phenotype. Ultimately, the mechanism of THC suppression of HIV-1 infection was traced to a reduction in cell surface HIV receptor (CD4, CCR5 and CXCR4) expression that diminished entry efficiency.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Anderson J, Akkina R (2005) HIV-1 resistance conferred by siRNA cosuppression of CXCR4 and CCR5 coreceptors by a bispecific lentiviral vector. AIDS Res Ther 2:1

    Article  PubMed Central  PubMed  Google Scholar 

  • Anderson J, Banerjea A, Akkina R (2003) Bispecific short hairpin siRNA constructs targeted to CD4, CXCR4, and CCR5 confer HIV-1 resistance. Oligonucleotides 13:303–312

    Article  CAS  PubMed  Google Scholar 

  • Ben Amar M (2006) Cannabinoids in medicine: a review of their therapeutic potential. J Ethnopharmacol 105:1–25

    Article  CAS  PubMed  Google Scholar 

  • Bergamaschi A, Pancino G (2010) Host hindrance to HIV-1 replication in monocytes and macrophages. Retrovirology 7:31

    Article  PubMed Central  PubMed  Google Scholar 

  • Bol SM, van Remmerden Y, Sietzema JG, Kootstra NA, Schuitemaker H, van’t Wout AB (2009) Donor variation in in vitro HIV-1 susceptibility of monocyte-derived macrophages. Virology 390:205–211

    Article  CAS  PubMed  Google Scholar 

  • Bouaboula M, Poinot-Chazel C, Marchand J, Canat X, Bourrié B, Rinaldi-Carmona M, Calandra B, Le Fur G, Casellas P (1996) Signaling pathway associated with stimulation of CB2 peripheral cannabinoid receptor. Involvement of both mitogen-activated protein kinase and induction of Krox-24 expression. Eur J Biochem 237:704–711

    Article  CAS  PubMed  Google Scholar 

  • Buchweitz JP, Karmaus PW, Harkema JR, Williams KJ, Kaminski NE (2007) Modulation of airway responses to influenza A/PR/8/34 by Delta9-tetrahydrocannabinol in C57BL/6 mice. J Pharmacol Exp Ther 323:675–683

    Article  CAS  PubMed  Google Scholar 

  • Buckner CM, Calderon TM, Willams DW, Belbin TJ, Berman JW (2011) Characterization of monocyte maturation/differentiation that facilitates their transmigration across the blood–brain barrier and infection by HIV: implications for NeuroAIDS. Cell Immunol 267:109–123

    Article  CAS  PubMed  Google Scholar 

  • Cabral GA, Griffin-Thomas L (2009) Emerging role of the cannabinoid receptor CB2 in immune regulation: therapeutic prospects for neuroinflammation. Exp Rev Mol Med 11:e3

    Article  Google Scholar 

  • Cabral GA, Marciano-Cabral F (2005) Cannabinoid receptors in microglia of the central nervous system: immune functional relevance. J Leukoc Biol 78:1192–1197

    Article  CAS  PubMed  Google Scholar 

  • Castaneda JT, Harui A, Kiertscher SM, Roth JD, Roth MD (2013) Differential expression of intracellular and extracellular CB(2) cannabinoid receptor protein by human peripheral blood leukocytes. J NeuroImmune Pharmacol 8:323–332

    Article  PubMed Central  PubMed  Google Scholar 

  • Castaño D, Barrera LF, Rojas M (2011) Mycobacterium tuberculosis alters the differentiation of monocytes into macrophages in vitro. Cell Immunol 268:60–67

    Article  PubMed  Google Scholar 

  • Chang YH, Lee ST, Lin WW (2001) Effects of cannabinoids on LPS-stimulated inflammatory mediator release from macrophages: involvement of eicosanoids. J Cell Biochem 81:715–723

    Article  CAS  PubMed  Google Scholar 

  • Chikere K, Chou T, Gorry PR, Lee B (2013) Affinofile profiling: how efficiency of CD4/CCR5 usage impacts the biological and pathogenic phenotype of HIV. Virology 435:81–91

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Coberley CR, Kohler JJ, Brown JN, Oshier JT, Baker HV, Popp MP, Sleasman JW, Goodenow MM (2004) Impact on genetic networks in human macrophages by a CCR5 strain of human immunodeficiency virus type 1. J Virol 78:11477–11486

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Coffey RG, Snella E, Johnson K, Pross S (1996) Inhibition of macrophage nitric oxide production by tetrahydrocannabinol in vivo and in vitro. Int J Immunopharmacol 18:749–752

    Article  CAS  PubMed  Google Scholar 

  • 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:e33961

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, Gibson D, Mandelbaum A, Etinger A, Mechoulam R (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 258:1946–1949

    Article  CAS  PubMed  Google Scholar 

  • Ellery PJ, Tippett E, Chiu YL, Paukovics G, Cameron PU, Solomon A, Lewin SR, Gorry PR, Jaworowski A, Greene WC, Sonza S, Crowe SM (2007) The CD16+ monocyte subset is more permissive to infection and preferentially harbors HIV-1 in vivo. J Immunol 178:6581–6589

    Article  CAS  PubMed  Google Scholar 

  • Fischer-Smith T, Tedaldi EM, Rappaport J (2008) CD163/CD16 coexpression by circulating monocytes/macrophages in HIV: potential biomarkers for HIV infection and AIDS progression. AIDS Res Hum Retrovir 24:417–421

    Article  CAS  PubMed  Google Scholar 

  • Galiègue S, Mary S, Marchand J, Dussossoy D, Carrière D, Carayon P, Bouaboula M, Shire D, Le Fur G, Casellas P (1995) Expression of central and peripheral cannabinoid receptors in human immune tissues and leukocyte subpopulations. Eur J Biochem 232:54–61

    Article  PubMed  Google Scholar 

  • Gendelman HE, Orenstein JM, Martin MA, Ferrua C, Mitra R, Phipps T, Wahl LA, Lane HC, Fauci AS, Burke DS (1988) Efficient isolation and propagation of human immunodeficiency virus on recombinant colony-stimulating factor 1-treated monocytes. J Exp Med 167:1428–1441

    Article  CAS  PubMed  Google Scholar 

  • Grotenhermen F (2003) Pharmacokinetics and pharmacodynamics of cannabinoids. Clin Pharmacokinet 42:327–360

    Article  CAS  PubMed  Google Scholar 

  • Han KH, Lim S, Ryu J, Lee CW, Kim Y, Kang JH, Kang SS, Ahn YK, Park CS, Kim JJ (2009) CB1 and CB2 cannabinoid receptors differentially regulate the production of reactive oxygen species by macrophages. Cardiovasc Res 84:378–386

    Article  CAS  PubMed  Google Scholar 

  • Henstridge CM, Balenga NA, Kargl J, Andradas C, Brown AJ, Irving A, Sanchez C, Waldhoer M (2011) Minireview: recent developments in the physiology and pathology of the lysophosphatidylinositol-sensitive receptor GPR55. Mol Endocrinol 25:1835–1848

    Article  CAS  PubMed  Google Scholar 

  • Ho BT, Fritchie GE, Kralik PM, Englert LF, McIsaac WM, Idänpään-Heikkilä J (1970) Distribution of tritiated-1 delta 9tetrahydrocannabinol in rat tissues after inhalation. J Pharm Pharmacol 22:538–539

    Article  CAS  PubMed  Google Scholar 

  • Huemer HP, Lassnig C, Bernhard D, Sturm S, Nowotny N, Kitchen M, Pavlic M (2011) Cannabinoids lead to enhanced virulence of the smallpox vaccine (vaccinia) virus. Immunobiology 216:670–677

    Article  CAS  PubMed  Google Scholar 

  • Hunt PW (2012) HIV and inflammation: mechanisms and consequences. Curr HIV/AIDS Rep 9:139–147

    Article  PubMed  Google Scholar 

  • Johnston SH, Lobritz MA, Nguyen S, Lassen K, Delair S, Posta F, Bryson YJ, Arts EJ, Chou T, Lee B (2009) A quantitative affinity-profiling system that reveals distinct CD4/CCR5 usage patterns among human immunodeficiency virus type 1 and simian immunodeficiency virus strains. J Virol 83:11016–11026

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, Salazar MG, Sun C, Grayson T, Wang S, Li H, Wei X, Jiang C, Kirchherr JL, Gao F, Anderson JA, Ping LH, Swanstrom R, Tomaras GD, Blattner WA, Goepfert PA, Kilby JM, Saag MS, Delwart EL, Busch MP, Cohen MS, Montefiori DC, Haynes BF, Gaschen B, Athreya GS, Lee HY, Wood N, Seoighe C, Perelson AS, Bhattacharya T, Korber BT, Hahn BH, Shaw GM (2008) Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 105:7552–7557

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Klein TW, Newton CA, Widen R, Friedman H (1985) The effect of delta-9-tetrahydrocannabinol and 11-hydroxy-delta-9-tetrahydrocannabinol on T-lymphocyte and B-lymphocyte mitogen responses. J Immunopharmacol 7:451–466

    Article  CAS  PubMed  Google Scholar 

  • Kreuz DS, Axelrod J (1973) Delta-9-tetrahydrocannabinol: localization in body fat. Science 179:391–393

    Article  CAS  PubMed  Google Scholar 

  • Lentz MR, Kim WK, Kim H, Soulas C, Lee V, Venna N, Halpern EF, Rosenberg ES, Williams K, González RG (2011) Alterations in brain metabolism during the first year of HIV infection. J Neurovirol 17:220–229

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lynn AB, Herkenham M (1994) Localization of cannabinoid receptors and nonsaturable high-density cannabinoid binding sites in peripheral tissues of the rat: implications for receptor-mediated immune modulation by cannabinoids. J Pharmacol Exp Ther 268:1612–1623

    CAS  PubMed  Google Scholar 

  • Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346:561–564

    Article  CAS  PubMed  Google Scholar 

  • McMahon SB, Monroe JG (1996) The role of early growth response gene 1 (egr-1) in regulation of the immune response. J Leukoc Biol 60:159–166

    CAS  PubMed  Google Scholar 

  • Medveczky MM, Sherwood TA, Klein TW, Friedman H, Medveczky PG (2004) Delta-9 tetrahydrocannabinol (THC) inhibits lytic replication of gamma oncogenic herpesviruses in vitro. BMC Med 2:34

    Article  PubMed Central  PubMed  Google Scholar 

  • Millard AL, Mertes PM, Ittelet D, Villard F, Jeannesson P, Bernard J (2002) Butyrate affects differentiation, maturation and function of human monocyte-derived dendritic cells and macrophages. Clin Exp Immunol 130:245–255

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 6:516–527

    Article  PubMed Central  PubMed  Google Scholar 

  • Molina PE, Winsauer P, Zhang P, Walker E, Birke L, Amedee A, Stouwe CV, Troxclair D, McGoey R, Varner K, Byerley L, LaMotte L (2011b) Cannabinoid administration attenuates the progression of simian immunodeficiency virus. AIDS Res Hum Retrovir 27:585–592

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • National Institute on Drug Abuse (2012) Research Report Series: Marijuana abuse. In: NIoD (ed) Abuse. National Institutes of Health

  • Newton CA, Klein TW (2012) Cannabinoid 2 (CB2) receptor involvement in the down-regulation but not up-regulation of serum IgE levels in immunized mice. J NeuroImmune Pharmacol 7:591–598

    Article  PubMed Central  PubMed  Google Scholar 

  • Nichols S, Lowe A, Zhange X, Garvie P, Thornton S, Goldberger B, Hou W, Goodenow M, Sleasman J (2014) Concordance between self-reported substance use and toxicoogy among HIV-infected and unifected at risk youth. Drug Alcohol Depend 134:376–382

    Google Scholar 

  • O’Connell O, Repik A, Reeves JD, Gonzalez-Perez MP, Quitadamo B, Anton ED, Duenas-Decamp M, Peters P, Lin R, Zolla-Pazner S, Corti D, Wallace A, Wang S, Kong XP, Lu S, Clapham PR (2013) Efficiency of bridging-sheet recruitment explains HIV-1 R5 envelope glycoprotein sensitivity to soluble CD4 and macrophage tropism. J Virol 87:187–198

    Article  PubMed Central  PubMed  Google Scholar 

  • Raborn ES, Cabral GA (2010) Cannabinoid inhibition of macrophage migration to the trans-activating (Tat) protein of HIV-1 is linked to the CB(2) cannabinoid receptor. J Pharmacol Exp Ther 333:319–327

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Raborn ES, Marciano-Cabral F, Buckley NE, Martin BR, Cabral GA (2008) The cannabinoid delta-9-tetrahydrocannabinol mediates inhibition of macrophage chemotaxis to RANTES/CCL5: linkage to the CB2 receptor. J NeuroImmune Pharmacol 3:117–129

    Article  PubMed Central  PubMed  Google Scholar 

  • Ramirez SH, Reichenbach NL, Fan S, Rom S, Merkel SF, Wang X, Ho WZ, Persidsky Y (2013) Attenuation of HIV-1 replication in macrophages by cannabinoid receptor 2 agonists. J Leukoc Biol 93:801–810

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rinehart JJ, Wuest D, Ackerman GA (1982) Corticosteroid alteration of human monocyte to macrophage differentiation. J Immunol 129:1436–1440

    CAS  PubMed  Google Scholar 

  • Rotheram-Borus MJ, Murphy DA, Coleman CL, Kennedy M, Reid HM, Cline TR, Birnbaum JM, Futterman D, Levin L, Schneir A, Chabon B, O’Keefe Z, Kipke M (1997) Risk acts, health care, and mdical adherence among HIV+ youths in care over time. AIDS Behav 1:43–52

    Article  Google Scholar 

  • Ryrfeldt A, Ramsay CH, Nilsson IM, Widman M, Agurell S (1973) Whole-body autoradiography of 1-tetrahydrocannabinol and 1(6)-tetrahydrocannabinol in mouse. Pharmacokinetic aspects of 1-tetrahydrocannabinol and its metabolites. Acta Pharm Suec 10:13–28

    CAS  PubMed  Google Scholar 

  • Sevigny EL (2013) Is today’s marijuana more potent simply because it’s fresher? Drug Test Anal 5:62–67

    Article  CAS  PubMed  Google Scholar 

  • Shivers SC, Newton C, Friedman H, Klein TW (1994) delta 9-tetrahydrocannabinol (THC) modulates IL-1 bioactivity in human monocyte/macrophage cell lines. Life Sci 54:1281–1289

    Article  CAS  PubMed  Google Scholar 

  • Springs AE, Karmaus PW, Crawford RB, Kaplan BL, Kaminski NE (2008) Effects of targeted deletion of cannabinoid receptors CB1 and CB2 on immune competence and sensitivity to immune modulation by delta9-tetrahydrocannabinol. J Leukoc Biol 84:1574–1584

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Surdo M, Balestra E, Saccomandi P, Di Santo F, Montano M, Di Carlo D, Sarmati L, Aquaro S, Andreoni M, Svicher V, Perno CF, Ceccherini-Silberstein F (2013) Inhibition of dual/mixed tropic HIV-1 isolates by CCR5-inhibitors in primary lymphocytes and macrophages. PLoS One 8:e68076

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tang JL, Lancz G, Specter S (1993) Delta-9-tetrahydrocannabinol-(THC)-mediated inhibition of macrophage macromolecular metabolism is antagonized by human serum proteins and by cell surface proteins. Int J Immunopharmacol 15:665–672

    Article  CAS  PubMed  Google Scholar 

  • Theodore TS, Englund G, Buckler-White A, Buckler CE, Martin MA, Peden KW (1996) Construction and characterization of a stable full-length macrophage-tropic HIV type 1 molecular clone that directs the production of high titers of progeny virions. AIDS Res Hum Retrovir 12:191–194

    Article  CAS  PubMed  Google Scholar 

  • Tuttle DL, Harrison JK, Anders C, Sleasman JW, Goodenow MM (1998) Expression of CCR5 increases during monocyte differentiation and directly mediates macrophage susceptibility to infection by human immunodeficiency virus type 1. J Virol 72:4962–4969

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tuttle DL, Anders CB, Aquino-De Jesus MJ, Poole PP, Lamers SL, Briggs DR, Pomeroy SM, Alexander L, Peden KW, Andiman WA, Sleasman JW, Goodenow MM (2002) Increased replication of non-syncytium-inducing HIV type 1 isolates in monocyte-derived macrophages is linked to advanced disease in infected children. AIDS Res Hum Retrovir 18:353–362

    Article  PubMed  Google Scholar 

  • Vindenes V, Strand DH, Kristoffersen L, Boix F, Mørland J (2013) Has the intake of THC by cannabis users changed over the last decade? Evidence of increased exposure by analysis of blood THC concentrations in impaired drivers. Forensic Sci Int 226:197–201

    Article  CAS  PubMed  Google Scholar 

  • Wallet MA, Rodriguez CA, Yin L, Saporta S, Chinratanapisit S, Hou W, Sleasman JW, Goodenow MM (2010) Microbial translocation induces persistent macrophage activation unrelated to HIV-1 levels or T-cell activation following therapy. AIDS 24:1281–1290

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wallet MA, Reist CM, Williams JC, Appelberg S, Guiulfo GL, Gardner B, Sleasman JW, Goodenow MM (2012) The HIV-1 protease inhibitor nelfinavir activates PP2 and inhibits MAPK signaling in macrophages: a pathway to reduce inflammation. J Leukoc Biol 92:795–805

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Watzl B, Scuderi P, Watson RR (1991) Marijuana components stimulate human peripheral blood mononuclear cell secretion of interferon-gamma and suppress interleukin-1 alpha in vitro. Int J Immunopharmacol 13:1091–1097

    Article  CAS  PubMed  Google Scholar 

  • Whyte LS, Ryberg E, Sims NA, Ridge SA, Mackie K, Greasley PJ, Ross RA, Rogers MJ (2009) The putative cannabinoid receptor GPR55 affects osteoclast function in vitro and bone mass in vivo. Proc Natl Acad Sci U S A 106:16511–16516

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Williams DW, Eugenin EA, Calderon TM, Berman JW (2012) Monocyte maturation, HIV susceptibility, and transmigration across the blood brain barrier are critical in HIV neuropathogenesis. J Leukoc Biol 91:401–415

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang X, Wang JF, Kunos G, Groopman JE (2007) Cannabinoid modulation of Kaposi’s sarcoma-associated herpesvirus infection and transformation. Cancer Res 67:7230–7237

    Article  CAS  PubMed  Google Scholar 

  • Zheng ZM, Specter S, Friedman H (1992) Inhibition by delta-9-tetrahydrocannabinol of tumor necrosis factor alpha production by mouse and human macrophages. Int J Immunopharmacol 14:1445–1452

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to acknowledge Daniel Rodriguez, Chris Little, and Steve Pomeroy for technical assistance and thank Dr. Mark Wallet for helpful comments and critical review of the manuscript. We would also like to thank the University of Florida Interdisciplinary Center for Biotechnology Research cellomics core facility for providing flow cytometers and genomics core facility for Sanger sequencing and access to the ABI 7500 FAST instrument. This study was supported in part by HHS funding from the National Institute for Drug Abuse [DA031017] and by Adolescent Medicine Trials Network for HIV/AIDS Interventions (ATN) supported by the National Institutes of Child Health and Development [HD40533 and HD40474]. JCW is supported by the Laura McClamma Fellowship at the University of Florida. SA is supported by the University of Florida Alumni graduate fellowship and the Linton E. Grinter fellowship. Additional support was provided by the Robert A. Good endowed Chair in Immunology (University of South Florida), Stephany W. Holloway University Chair for AIDS Research (University of Florida), Center for Research in Pediatric Immune Deficiency and Inflammation, and University of Florida Health Cancer Center.

Conflict of Interest

The authors declare that we have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Pathology, Immunology and Laboratory Medicine, College of Medicine, University of Florida, 2033 Mowry Road, Campus Box 103633, Gainesville, FL, 32610-3663, USA

    Julie C. Williams, Sofia Appelberg, Bruce A. Goldberger & Maureen M. Goodenow

  2. Department of Molecular Medicine, University of South Florida, Tampa, FL, USA

    Thomas W. Klein

  3. Department of Pediatrics, Division of Allergy and Immunology, School of Medicine, Duke University, DUMC Box 2644, Durham, NC, 27710, USA

    John W. Sleasman

Authors
  1. Julie C. Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sofia Appelberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bruce A. Goldberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thomas W. Klein
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. John W. Sleasman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maureen M. Goodenow
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maureen M. Goodenow.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Williams, J.C., Appelberg, S., Goldberger, B.A. et al. Δ9-Tetrahydrocannabinol Treatment During Human Monocyte Differentiation Reduces Macrophage Susceptibility to HIV-1 Infection. J Neuroimmune Pharmacol 9, 369–379 (2014). https://doi.org/10.1007/s11481-014-9527-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11481-014-9527-3

Keywords

Search

Navigation