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Review Article

Extracellular vesicles and chronic inflammation during HIV infection

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Article: 1687275 | Received 25 Jul 2019, Accepted 23 Oct 2019, Published online: 06 Nov 2019

References

  • World Health Organization. HIV/AIDS [Internet]; 2018 [cited 2019 Jul 22]. Available from: https://www.who.int/en/news-room/fact-sheets/detail/hiv-aids
  • Riddler SA, Aga E, Bosch RJ, et al. Continued slow decay of the residual plasma viremia level in HIV-1 – infected adults receiving long-term antiretroviral therapy. J Infect Dis. 2016;213(4):556–16.
  • Maldarelli F, Palmer S, King MS, et al. ART suppresses plasma HIV-1 RNA to a stable set point predicted by pretherapy viremia. PLoS Pathog. 2007;3(4):e46.
  • Neuhaus J, Jacobs, Jr DR Jr, Baker JV, et al. Markers of inflammation, coagulation, and renal function are elevated in adults with HIV infection. J Infect Dis. 2012;42(12):3334–3345.
  • Wada NI, Jacobson LP, Margolick JB, et al. The effect of HAART-induced HIV suppression on circulating markers of inflammation and immune activation. AIDS. 2015;29(4):463–471.
  • Tenorio AR, Zheng Y, Bosch RJ, et al. Soluble markers of inflammation and coagulation but not T-cell activation predict non-AIDS-defining morbid events during suppressive antiretroviral treatment. J Infect Dis. 2014;210(8):1248–1259.
  • Hsue PY, Deeks SG, Hunt PW. Immunologic basis of cardiovascular disease in HIV-infected adults. J Infect Dis. 2012;205(SUPPL. 3):375–382.
  • Marks MA, Rabkin CS, Engels EA, et al. Markers of microbial translocation and risk of AIDS-related lymphoma. AIDS. 2013 Jan;27(3):469–474.
  • Ancuta P, Kamat A, Kunstman KJ, et al. Microbial translocation is associated with increased monocyte activation and dementia in AIDS patients. PLoS One. 2008;3(6):e2516.
  • Andrade BB, Hullsiek KH, Boulware DR, et al. Biomarkers of inflammation and coagulation are associated with mortality and hepatitis flares in persons coinfected with HIV and hepatitis viruses. J Infect Dis. 2013;207(9):1379–1388.
  • Kuller LH, Lundgren J, Neaton JD, et al. Inflammatory and coagulation biomarkers and mortality in patients with HIV infection. PLoS Med. 2008;5(10):e203.
  • Brenchley JM, Price DA, Schacker TW, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med. 2006 Dec;12(12):1365–1371.
  • Martinez-Picado J, Deeks SG. Persistent HIV-1 replication during antiretroviral therapy. Curr Opin HIV AIDS. 2016;11(4):417–423.
  • Gianella S, Letendre S. Cytomegalovirus and HIV: a dangerous Pas de Deux. J Infect Dis. 2016;214(Suppl 2):S67–74.
  • Hunt PW, Landay AL, Sinclair E, et al. A low T regulatory cell response may contribute to both viral control and generalized immune activation in HIV controllers. PLoS One. 2011 Jan;6(1):e15924.
  • Estes JD, Haase AT, Schacker TW. The role of collagen deposition in depleting CD4+ T cells and limiting reconstitution in HIV-1 and SIV infections through damage to the secondary lymphoid organ niche. Semin Immunol. 2008;20(3):181–186.
  • Witwer KW, Théry C. Extracellular vesicles or exosomes? On primacy, precision, and popularity influencing a choice of nomenclature. J Extracell Vesicles [Internet]. 2019;8(1):1648167.
  • Mathieu M, Martin-Jaular L, Lavieu G, et al. Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication [Internet]. Nat Cell Biol. 2019;21(1):9–17. Available from: http://www.nature.com/articles/s41556-018-0250-9.
  • Minciacchi VR, You S, Spinelli C, et al. Large oncosomes contain distinct protein cargo and represent a separate functional class of tumor-derived extracellular vesicles. Oncotarget. 2015 May;6(13):11327–11341.
  • Keerthikumar S, Gangoda L, Liem M, et al. Proteogenomic analysis reveals exosomes are more oncogenic than ectosomes. Oncotarget. 2015 Jun;6(17):15375–15396.
  • Mateescu B, Kowal EJK, van Balkom BWM, et al. Obstacles and opportunities in the functional analysis of extracellular vesicle RNA - an ISEV position paper. J Extracell Vesicles. 2017;6(1):1286095.
  • Yanez-Mo M, Siljander PR-M, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4:27066.
  • Théry C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 2009;9(8):581–593.
  • Robbins PD, Morelli AE. Regulation of immune responses by extracellular vesicles. Nat Rev Immunol [Internet]. 2014;14(3):195–208.
  • Théry C, Duban L, Segura E, et al. Indirect activation of naïve CD4+T cells by dendritic cell-derived exosomes. Nat Immunol. 2002;3(12):1156–1162.
  • Zitvogel L, Regnault A, Lozier A, et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med. 1998 May;4(5):594–600.
  • Tkach M, Kowal J, Zucchetti AE, et al. Qualitative differences in T-cell activation by dendritic cell-derived extracellular vesicle subtypes. EMBO J. 2017;36(20):3012–3028.
  • Okoye IS, Coomes SM, Pelly VS, et al. MicroRNA-containing T-regulatory-cell-derived exosomes suppress pathogenic T helper 1 cells. Immunity. 2014 Jul;41(1):89–103.
  • Zhang F, Li R, Yang Y, et al. Specific decrease in B-cell-derived extracellular vesicles enhances post-chemotherapeutic CD8+ T cell responses. Immunity. [Internet]. 2019 Feb 12: pii: S1074. [cited 2019 Mar 8]. Available from: https://www.sciencedirect.com/science/article/pii/S1074761319300330?via%3Dihub
  • Turpin D, Truchetet ME, Faustin B, et al. Role of extracellular vesicles in autoimmune diseases. Autoimmun Rev [Internet]. 2016;15(2):174–183.
  • Kim M-R, Hong S-W, Choi E-B, et al. Staphylococcus aureus-derived extracellular vesicles induce neutrophilic pulmonary inflammation via both Th1 and Th17 cell responses. Allergy. 2012 Oct;67(10):1271–1281.
  • Hong S-W, Kim M-R, Lee E-Y, et al. Extracellular vesicles derived from staphylococcus aureus induce atopic dermatitis-like skin inflammation. Allergy. 2011 Mar;66(3):351–359.
  • Nakao R, Hasegawa H, Ochiai K, et al. Outer membrane vesicles of porphyromonas gingivalis elicit a mucosal immune response. PLoS One. 2011;6(10):e26163.
  • Prados-Rosales R, Baena A, Martinez LR, et al. Mycobacteria release active membrane vesicles that modulate immune responses in a TLR2-dependent manner in mice. J Clin Invest. 2011 Apr;121(4):1471–1483.
  • Bhatnagar S, Shinagawa K, Castellino FJ, et al. Exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and in vivo exosomes released from macrophages infected with intracellular pathogens stimulate a proinflammatory response in vitro and i. Blood. 2007;110(9):3234–3244.
  • Singh PP, LeMaire C, Tan JC, et al. Exosomes released from M. tuberculosis infected cells can suppress IFN-gamma mediated activation of naive macrophages. PLoS One. 2011 Apr;6(4):e18564.
  • Ayna G, Krysko DV, Kaczmarek A, et al. ATP release from dying autophagic cells and their phagocytosis are crucial for inflammasome activation in macrophages. PLoS One. 2012;7(6):e40069.
  • Goh FG, Midwood KS. Intrinsic danger: activation of toll-like receptors in rheumatoid arthritis. Rheumatology (Oxford). 2012 Jan;51(1):7–23.
  • Gulinelli S, Salaro E, Vuerich M, et al. IL-18 associates to microvesicles shed from human macrophages by a LPS/TLR-4 independent mechanism in response to P2X receptor stimulation. Eur J Immunol. 2012 Dec;42(12):3334–3345.
  • Nickel W, Rabouille C. Mechanisms of regulated unconventional protein secretion. Nat Rev Mol Cell Biol. 2009 Feb;10(2):148–155.
  • Pizzirani C, Ferrari D, Chiozzi P, et al. Stimulation of P2 receptors causes release of IL-1 β − loaded microvesicles from human dendritic cells. Blood. 2012;109(9):3856–3864.
  • Cossetti C, Iraci N, Mercer TR, et al. Extracellular vesicles from neural stem cells transfer IFN-gamma via Ifngr1 to activate Stat1 signaling in target cells. Mol Cell. 2014 Oct;56(2):193–204.
  • Esser J, Gehrmann U, D’Alexandri FL, et al. Exosomes from human macrophages and dendritic cells contain enzymes for leukotriene biosynthesis and promote granulocyte migration. J Allergy Clin Immunol. 2010 Nov;126(5):1032–1040. 1040.e1–4.
  • Majumdar R, Tavakoli Tameh A, Parent CA. Exosomes mediate LTB4 release during neutrophil chemotaxis. PLoS Biol. 2016 Jan;14(1):e1002336.
  • Kriebel PW, Majumdar R, Jenkins LM, et al. Extracellular vesicles direct migration by synthesizing and releasing chemotactic signals. J Cell Biol. 2018 Aug;217(8):2891–2910.
  • Bello-Morales R, Praena B, de la Nuez C, et al. Role of microvesicles in the spread of herpes simplex virus 1 in oligodendrocytic cells. J Virol. 2018;92(10):1–19.
  • Yang Y, Han Q, Hou Z, et al. Exosomes mediate hepatitis B virus (HBV) transmission and NK-cell dysfunction. Cell Mol Immunol [Internet]. 2017;14(5):465–475.
  • Bukong TN, Momen-Heravi F, Kodys K, et al. Exosomes from hepatitis C infected patients transmit HCV infection and contain replication competent viral RNA in complex with Ago2-miR122-HSP90. PLoS Pathog. 2014;10(10):e1004424.
  • Ramakrishnaiah V, Thumann C, Fofana I, et al. Exosome-mediated transmission of hepatitis C virus between human hepatoma Huh7.5 cells. Proc Natl Acad Sci. 2013;110(32):13109–13113.
  • Feng Z, Hensley L, McKnight KL, et al. A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature [Internet]. 2013;496(7445):367–371.
  • Chen Y-H, Du W, Hagemeijer MC, et al. Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses. Cell. 2015 Feb;160(4):619–630.
  • Santiana M, Ghosh S, Ho BA, et al. Vesicle-cloaked virus clusters are optimal units for inter-organismal viral transmission. Cell Host Microbe. 2018;24(2):208–220.e8.
  • van der Grein SG, Defourny KAY, Rabouw HH, et al. Picornavirus infection induces temporal release of multiple extracellular vesicle subsets that differ in molecular composition and infectious potential. PLOS Pathog [Internet]. 2019;15(2):e1007594. Available from: http://dx.plos.org/10.1371/journal.ppat.1007594.
  • Dukers DF, Meij P, Vervoort MBHJ, et al. Direct immunosuppressive effects of EBV-encoded latent membrane protein 1. J Immunol. 2000;165(2):663–670.
  • Keryer-Bibens C, Pioche-Durieu C, Villemant C, et al. Exosomes released by EBV-infected nasopharyngeal carcinoma cells convey the viral latent membrane protein 1 and the immunomodulatory protein galectin 9. BMC Cancer. 2006;6:1–8.
  • Fu Y, Zhang L, Zhang F, et al. Exosome-mediated miR-146a transfer suppresses type I interferon response and facilitates EV71 infection. PLoS Pathog. 2017;13(9):1–31.
  • Klibi J, Niki T, Riedel A, et al. Blood diffusion and Th1-suppressive effects of galectin-9-containing exosomes released by Epstein-Barr virus-infected nasopharyngeal carcinoma cells. Blood. 2009;113(9):1957–1967.
  • Cobb DA, Kim OK, Golden-Mason L, et al. Hepatocyte-derived exosomes promote T follicular regulatory cell expansion during hepatitis C virus infection. Hepatology. 2018;67(1):71–85.
  • Feng Z, Walker CM, Lemon SM, et al. Human pDCs preferentially sense enveloped hepatitis A virions. J Clin Invest. 2015;125(1):169–176.
  • Dreux M, Garaigorta U, Boyd B, et al. Short-range exosomal transfer of viral RNA from infected cells to plasmacytoid dendritic cells triggers innate immunity. Cell Host Microbe. 2012;12(4):558–570.
  • Baglio SR, van Eijndhoven MAJ, Koppers-Lalic D, et al. Sensing of latent EBV infection through exosomal transfer of 5′pppRNA. Proc Natl Acad Sci. 2016;113(5):E587–96.
  • Li J, Liu K, Liu Y, et al. Exosomes mediate the cell-to-cell transmission of IFN-α-induced antiviral activity. Nat Immunol. 2013;14(8):793–803.
  • Deschamps T, Kalamvoki M. Extracellular vesicles released by herpes simplex virus 1-infected cells block virus replication in recipient cells in a STING-dependent manner. J Virol. 2018 Sep;92(18):e01102-18.
  • Delorme-Axford E, Donker RB, Mouillet JF, et al. Human placental trophoblasts confer viral resistance to recipient cells. Proc Natl Acad Sci U S A. 2013;110(29):12048–12053.
  • Gould SJ, Booth AM, Hildreth JEK. The Trojan exosome hypothesis. Proc Natl Acad Sci U S A. 2003 Sep;100(19):10592–10597.
  • Bess JWJ, Gorelick RJ, Bosche WJ, et al. Microvesicles are a source of contaminating cellular proteins found in purified HIV-1 preparations. Virology. 1997 Mar;230(1):134–144.
  • Nolte-’t Hoen E, Cremer T, Gallo RC, et al. Extracellular vesicles and viruses: are they close relatives? Proc Natl Acad Sci U S A. 2016 Aug;113(33):9155–9161.
  • Ott DE. Purification of HIV-1 virions by subtilisin digestion or CD45 immunoaffinity depletion for biochemical studies. Methods Mol Biol. 2009;485:15–25.
  • Cantin R, Diou J, Bélanger D, et al. Discrimination between exosomes and HIV-1: purification of both vesicles from cell-free supernatants. J Immunol Methods. 2008;338(1–2):21–30.
  • Liao Z, Martin-Jaular L, Soueidi E, et al. Acetylcholinesterase is not a generic marker of extracellular vesicles. J Extracell Vesicles. 2019;8(1):1628592.
  • Théry C, Witwer KW, Aikawa E, et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the international society for extracellular vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles Internet]. 2018;8(1):1535750. Available from: https://www.tandfonline.com/doi/full/10.1080/20013078.2018.1535750
  • Böing AN, Van Der Pol E, Grootemaat AE, et al. Single-step isolation of extracellular vesicles from plasma by size-exclusion chromatography. Int Meet ISEV Rotterdam. 2014;3:118.
  • Karimi N, Cvjetkovic A, Jang SC, et al. Detailed analysis of the plasma extracellular vesicle proteome after separation from lipoproteins. Cell Mol Life Sci [Internet]. 2018;75(15):2873–2886.
  • Dias MVS, Costa CS, Da Silva LLP. The ambiguous roles of extracellular vesicles in HIV replication and pathogenesis. Front Microbiol. 2018;9(OCT):1–13.
  • de Carvalho JV, de Castro RO, da Silva EZM, et al. Nef neutralizes the ability of exosomes from CD4+ T cells to act as decoys during HIV-1 infection. PLoS One. 2014;9(11):e113691.
  • Khatua AK, Taylor HE, Hildreth JEK, et al. Exosomes packaging APOBEC3G confer human immunodeficiency virus resistance to recipient cells. J Virol. 2009 Jan;83(2):512–521.
  • Haque S, Sinha N, Ranjit S, et al. Monocyte-derived exosomes upon exposure to cigarette smoke condensate alter their characteristics and show protective effect against cytotoxicity and HIV-1 replication. Sci Rep [Internet]. 2017;7(1):1–14.
  • Tumne A, Prasad VS, Chen Y, et al. Noncytotoxic suppression of human immunodeficiency virus type 1 transcription by exosomes secreted from CD8+ T cells. J Virol. 2009 May;83(9):4354–4364.
  • Madison MN, Jones PH, Okeoma CM. Exosomes in human semen restrict HIV-1 transmission by vaginal cells and block intravaginal replication of LP-BM5 murine AIDS virus complex. Virology. 2015 Aug;482:189–201.
  • Madison MN, Roller RJ, Okeoma CM. Human semen contains exosomes with potent anti-HIV-1 activity. Retrovirology. 2014 Nov;11:102.
  • Verhoef K, Tijms M, Berkhout B. Optimal Tat-mediated activation of the HIV-1 LTR promoter requires a full-length TAR RNA hairpin. Nucleic Acids Res. 1997 Feb;25(3):496–502.
  • Welch JL, Kaddour H, Schlievert PM, et al. Semen exosomes promote transcriptional silencing of HIV-1 by disrupting NF-kappaB/Sp1/Tat circuitry. J Virol. 2018 Nov;92(21):e00731-18.
  • Naslund TI, Paquin-Proulx D, Paredes PT, et al. Exosomes from breast milk inhibit HIV-1 infection of dendritic cells and subsequent viral transfer to CD4+ T cells. AIDS. 2014 Jan;28(2):171–180.
  • Smith JA, Daniel R. Human vaginal fluid contains exosomes that have an inhibitory effect on an early step of the HIV-1 life cycle. AIDS. 2016 Nov;30(17):2611–2616.
  • Rozmyslowicz T, Majka M, Kijowski J, et al. Platelet- and megakaryocyte-derived microparticles transfer CXCR4 receptor to CXCR4-null cells and make them susceptible to infection by X4-HIV. AIDS. 2003 Jan;17(1):33–42.
  • Mack M, Kleinschmidt A, Bruhl H, et al. Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection. Nat Med. 2000 Jul;6(7):769–775.
  • Mercier SK, Donaghy H, Botting RA, et al. The microvesicle component of HIV-1 inocula modulates dendritic cell infection and maturation and enhances adhesion to and activation of T lymphocytes. PLoS Pathog. 2013 Oct;9(10):e1003700.
  • Kadiu I, Narayanasamy P, Dash PK, et al. Biochemical and biologic characterization of exosomes and microvesicles as facilitators of HIV-1 infection in macrophages. J Immunol [Internet]. 2012;189(2):744–754. Available from: http://www.jimmunol.org/cgi/doi/10.4049/jimmunol.1102244
  • Lenassi M, Cagney G, Liao M, et al. HIV Nef is secreted in exosomes and triggers apoptosis in bystander CD4+ T cells. Traffic. 2010;11(1):110–122.
  • Arenaccio C, Chiozzini C, Columba-Cabezas S, et al. Exosomes from human immunodeficiency virus type 1 (HIV-1)-infected cells license quiescent CD4+ T lymphocytes to replicate HIV-1 through a Nef- and ADAM17-dependent mechanism. J Virol. 2014 Oct;88(19):11529–11539.
  • Arakelyan A, Fitzgerald W, Zicari S, et al. Extracellular vesicles carry hiv env and facilitate HIV infection of human lymphoid tissue. Sci Rep. 2017 May;7(1):1695.
  • Narayanan A, Iordanskiy S, Das R, et al. Exosomes derived from HIV-1-infected cells contain trans-activation response element RNA. J Biol Chem. 2013;288(27):20014–20033.
  • Siliciano JD, Kajdas J, Finzi D, et al. Long-term follow-up studies confirm the stability of the latent reservoir for HIV-1 in resting CD4+ T cells. Nat Med. 2003 Jun;9(6):727–728.
  • Barclay RA, Schwab A, DeMarino C, et al. Exosomes from uninfected cells activate transcription of latent HIV-1. J Biol Chem. 2017 Jul;292(28):11682–11701.
  • Arenaccio C, Anticoli S, Manfredi F, et al. Latent HIV-1 is activated by exosomes from cells infected with either replication-competent or defective HIV-1. Retrovirology. 2015;12(1):1–17.
  • Tang X, Lu H, Dooner M, et al. Exosomal Tat protein activates latent HIV-1 in primary, resting CD4+ T lymphocytes. JCI Insight. 2018 Apr;3(7):95676.
  • Liao Z, Muth DC, Eitan E, et al. Serum extracellular vesicle depletion processes affect release and infectivity of HIV-1 in culture. Sci Rep. 2017 May;7(1):2558.
  • Buzas EI, György B, Nagy G, et al. Emerging role of extracellular vesicles in inflammatory diseases. Nat Rev Rheumatol [Internet]. 2014;10(6):356–364.
  • Boulanger CM, Loyer X, Rautou PE, et al. Extracellular vesicles in coronary artery disease. Nat Rev Cardiol [Internet]. 2017;14(5):259–272.
  • Lee JH, Schierer S, Blume K, et al. HIV-Nef and ADAM17-containing plasma extracellular vesicles induce and correlate with immune pathogenesis in chronic HIV infection. EBioMedicine [Internet]. 2016;6(1):03–13.
  • Chettimada S, Lorenz DR, Misra V, et al. Exosome markers associated with immune activation and oxidative stress in HIV patients on antiretroviral therapy. Sci Rep. 2018;8:7227.
  • Hubert A, Subra C, Jenabian MA, et al. Elevated abundance, size, and MicroRNA content of plasma extracellular vesicles in viremic HIV-1+ patients: correlations with known markers of disease progression. J Acquir Immune Defic Syndr. 2015;70(3):219–227.
  • Beck SE, Queen SE, Metcalf Pate KA, et al. An SIV/macaque model targeted to study HIV-associated neurocognitive disorders. J Neurovirol. 2018 Apr;24(2):204–212.
  • Koliha N, Wiencek Y, Heider U, et al. A novel multiplex bead-based platform highlights the diversity of extracellular vesicles. J Extracell Vesicles. 2016;5:29975.
  • Muratori C, Cavallin LE, Krätzel K, et al. Massive secretion by T cells is caused by HIV Nef in infected cells and by Nef transfer to bystander cells. Cell Host Microbe. 2009;6(3):218–230.
  • Subra C, Simard S, Mercier S, et al. Dendritic cells pulsed with HIV-1 release exosomes that promote apoptosis in CD4 + T lymphocytes. J Clin Cell Immunol [Internet]. 2011;7(1).
  • Mfunyi CM, Vaillancourt M, Vitry J, et al. Exosome release following activation of the dendritic cell immunoreceptor: a potential role in HIV-1 pathogenesis. Virology [Internet]. 2015;484:103–112.
  • Hromada C, Mühleder S, Grillari J, et al. Endothelial extracellular vesicles-promises and challenges. Front Physiol. 2017 May;8:275.
  • Bernard MA, Zhao H, Yue SC, et al. Novel HIV-1 MiRNAs stimulate TNFa release in human macrophages via TLR8 signaling pathway. PLoS One. 2014;9(9):e106006.
  • Lee JH, Wittki S, Bräu T, et al. HIV Nef, paxillin, and Pak1/2 regulate activation and secretion of TACE/ADAM10 proteases. Mol Cell. 2013;49(4):668–679.
  • Ostalecki C, Wittki S, Lee JH, et al. HIV Nef- and Notch1-dependent endocytosis of ADAM17 induces vesicular TNF secretion in chronic HIV infection. EBioMedicine [Internet]. 2016;13:294–304.
  • Duette G, Pereyra Gerber P, Rubione J, et al. Induction of HIF-1α by HIV-1 infection in CD4+ T cells promotes viral replication and drives extracellular vesicle-mediated inflammation. MBio [Internet]. 2018;9(5):e00757–18.
  • McNamara RP, Costantini LM, Myers TA, et al. Nef secretion into extracellular vesicles or exosomes is conserved across human and simian immunodeficiency viruses. MBio. 2018;9(1):1–20.
  • Raymond AD, Campbell-Sims TC, Khan M, et al. HIV type 1 Nef is released from infected cells in CD45+ microvesicles and is present in the plasma of HIV-infected individuals. AIDS Res Hum Retroviruses [Internet]. 2011;27(2):167–178. Available from: http://www.liebertonline.com/doi/abs/10.1089/aid.2009.0170
  • Luo X, Fan Y, Park IW, et al. Exosomes are unlikely involved in intercellular Nef transfer. PLoS One. 2015;10(4):1–25.
  • Columba Cabezas S, Federico M. Sequences within RNA coding for HIV-1 Gag p17 are efficiently targeted to exosomes. Cell Microbiol. 2013;15(3):412–429.
  • Sampey GC, Saifuddin M, Schwab A, et al. Exosomes from HIV-1-infected cells stimulate production of pro-inflammatory cytokines through trans-activating response (TAR) RNA. J Biol Chem. 2016;291(3):1251–1266.
  • Konadu KA, Huang MB, Roth W, et al. Isolation of exosomes from the plasma of HIV-1 positive individuals. J Vis Exp [Internet]. 2016;(107):1–9. Available from: http://www.jove.com/video/53495/isolation-of-exosomes-from-the-plasma-of-hiv-1-positive-individuals
  • Kodidela S, Ranjit S, Sinha N, et al. Cytokine profiling of exosomes derived from the plasma of HIV-infected alcohol drinkers and cigarette smokers. PLoS One. 2018;13(7):e0201144.
  • Swaminathan G, Navas-Martin S, Martin-Garcia J. MicroRNAs and HIV-1 infection: antiviral activities and beyond. J Mol Biol. 2014 Mar;426(6):1178–1197.
  • Huang J, Wang F, Argyris E, et al. Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes. Nat Med. 2007 Oct;13(10):1241–1247.
  • Roth WW, Huang MB, Konadu KA, et al. Micro RNA in exosomes from HIV-infected macrophages. Int J Environ Res Public Health. 2015;13(1):ijerph13010032.
  • Tang B, Li X, Ren Y, et al. MicroRNA-29a regulates lipopolysaccharide (LPS)-induced inflammatory responses in murine macrophages through the Akt1/NF-κB pathway. Exp Cell Res. 2017;360(2):74–80.
  • Semenza GL, Wang GL. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol. 1992 Dec;12(12):5447–5454.
  • Cramer T, Yamanishi Y, Clausen BE, et al. HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell. 2003 Mar;112(5):645–657.
  • Zhang W, Petrovic J-M, Callaghan D, et al. Evidence that hypoxia-inducible factor-1 (HIF-1) mediates transcriptional activation of interleukin-1beta (IL-1beta) in astrocyte cultures. J Neuroimmunol. 2006 May;174(1–2):63–73.
  • Cheng S-C, Quintin J, Cramer RA, et al. mTOR- and HIF-1alpha-mediated aerobic glycolysis as metabolic basis for trained immunity. Science. 2014 Sep;345(6204):1250684.
  • Wang T, Gilkes DM, Takano N, et al. Hypoxia-inducible factors and RAB22A mediate formation of microvesicles that stimulate breast cancer invasion and metastasis. Proc Natl Acad Sci. 2014;111(31):E3234–42.
  • Aga M, Bentz GL, Raffa S, et al. Exosomal HIF1alpha supports invasive potential of nasopharyngeal carcinoma-associated LMP1-positive exosomes. Oncogene. 2014 Sep;33(37):4613–4622.
  • Gonzalez-King H, Garcia NA, Ontoria-Oviedo I, et al. Hypoxia inducible factor-1alpha potentiates jagged 1-mediated angiogenesis by mesenchymal stem cell-derived exosomes. Stem Cells. 2017 Jul;35(7):1747–1759.
  • Chen F, Chen J, Yang L, et al. Extracellular vesicle-packaged HIF-1alpha-stabilizing lncRNA from tumour-associated macrophages regulates aerobic glycolysis of breast cancer cells. Nat Cell Biol. 2019 Apr;21(4):498–510.
  • Saylor D, Dickens AM, Sacktor N, et al. HIV-associated neurocognitive disorder — pathogenesis and prospects for treatment. Nat Rev Neurol. 2016 Apr;12(4):234–248.
  • Shaw G, Harper M, Hahn B, et al. HTLV-III infection in brains of children and adults with AIDS encephalopathy. Science. 1985 Jan;227(4683):177–182.
  • Hong S, Banks WA. Role of the immune system in HIV-associated neuroinflammation and neurocognitive implications. Brain Behav Immun. 2015 Mar;45:1–12.
  • Sillman B, Woldstad C, Mcmillan J, et al. Neuropathogenesis of human immunodeficiency virus infection. Handb Clin Neurol. 2018;152:21–40.
  • Witwer KW, Gama L, Li M, et al. Coordinated regulation of SIV replication and immune responses in the CNS. PLoS One. 2009 Dec 19;4(12):e8129.
  • Bissel SJ, Wiley CA. Human immunodeficiency virus infection of the brain: pitfalls in evaluating infected/affected cell populations. Brain Pathol. 2004 Jan;14(1):97–108.
  • Fischer-Smith T, Bell C, Croul S, et al. Monocyte/macrophage trafficking in acquired immunodeficiency syndrome encephalitis: lessons from human and nonhuman primate studies. J Neurovirol. 2008 Jan;14(4):318–326.
  • Williams KC, Corey S, Westmoreland SV, et al. Perivascular macrophages are the primary cell type productively infected by simian immunodeficiency virus in the brains of macaques: implications for the neuropathogenesis of AIDS. J Exp Med. 2001 April 17;193(8):905–915.
  • Cosenza MA, Zhao M-L, Si Q, et al. Human brain parenchymal microglia express CD14 and CD45 and are productively infected by HIV-1 in HIV-1 encephalitis. Brain Pathol. 2006 Apr;12(4):442–455.
  • Borjabad A, Brooks AI, Volsky DJ. Gene expression profiles of HIV-1-infected glia and brain: toward better understanding of the role of astrocytes in HIV-1-associated neurocognitive disorders. J Neuroimmune Pharmacol. 2010 Mar;5(1):44–62.
  • Ivey NS, MacLean AG, Lackner AA. Acquired immunodeficiency syndrome and the blood-brain barrier. J Neurovirol. 2009 Apr;15(2):111–122.
  • Tyor WR, Glass JD, Griffin JW, et al. Cytokine expression in the brain during the acquired immunodeficiency syndrome. Ann Neurol. 1992 Apr;31(4):349–360.
  • Lipton SA, Yeh M, Dreyer EB. Update on current models of HIV-related neuronal injury: platelet-activating factor, arachidonic acid and nitric oxide. Adv Neuroimmunol. 1994;4(3):181–188.
  • Alonso K, Pontiggia P, Medenica R, et al. Cytokine patterns in adults with AIDS. Immunol Invest. 1997 Apr;26(3):341–350.
  • Tavazzi E, Morrison D, Sullivan P, et al. Brain inflammation is a common feature of HIV-infected patients without HIV encephalitis or productive brain infection. Curr HIV Res. 2014;12(2):97–110.
  • Antinori A, Arendt G, Becker JT, et al. Updated research nosology for HIV-associated neurocognitive disorders. Neurology. 2007 Oct 05;69(18):1789–1799.
  • Wang T, Gong N, Liu J, et al. HIV-1-infected astrocytes and the microglial proteome. J Neuroimmune Pharmacol. 2008 Sep;3(3):173–186.
  • Yang L, Niu F, Yao H, et al. Exosomal miR-9 released from HIV Tat stimulated astrocytes mediates microglial migration. J Neuroimmune Pharmacol. 2018;13(3):330–344.
  • Ranjit S, Patters BJ, Gerth KA, et al. Potential neuroprotective role of astroglial exosomes against smoking-induced oxidative stress and HIV-1 replication in the central nervous system. Expert Opin Ther Targets. 2018 Aug;22(8):703–714.
  • Chaudhuri AD, Dastgheyb RM, Yoo S-W, et al. TNFα and IL-1β modify the miRNA cargo of astrocyte shed extracellular vesicles to regulate neurotrophic signaling in neurons article. Cell Death Dis. 2018;9(3):363.
  • Dickens AM, Tovar-y-Romo LB, Yoo S-W, et al. Astrocyte-shed extracellular vesicles regulate the peripheral leukocyte response to inflammatory brain lesions. Sci Signal. 2017 Apr;10(473):eaai7696.
  • Goetzl EJ, Schwartz JB, Abner EL, et al. High complement levels in astrocyte-derived exosomes of Alzheimer disease. Ann Neurol. 2018 Mar;83(3):544–552.
  • Pulliam L, Sun B, Mustapic M, et al. Plasma neuronal exosomes serve as biomarkers of cognitive impairment in HIV infection and Alzheimer’s disease. J Neurovirol. 2019 Jan. doi: 10.1007/s13365-018-0695-4. [Epub ahead of print].
  • Zhao J, Lopez AL, Erichsen D, et al. Mitochondrial glutaminase enhances extracellular glutamate production in HIV-1-infected macrophages: linkage to HIV-1 associated dementia. J Neurochem. 2003 Nov;88(1):169–180.
  • Wang K, Ye L, Lu H, et al. TNF-α promotes extracellular vesicle release in mouse astrocytes through glutaminase. J Neuroinflammation. 2017 Dec;14(1):87.
  • Wu B, Huang Y, Braun AL, et al. Glutaminase-containing microvesicles from HIV-1-infected macrophages and immune-activated microglia induce neurotoxicity. Mol Neurodegener. 2015 Dec;10(1):61.
  • Wu B, Liu J, Zhao R, et al. Glutaminase 1 regulates the release of extracellular vesicles during neuroinflammation through key metabolic intermediate alpha-ketoglutarate. J Neuroinflammation. 2018;15(1):1–14.
  • Ye L, Huang Y, Zhao L, et al. IL-1β and TNF-α induce neurotoxicity through glutamate production: a potential role for neuronal glutaminase. J Neurochem. 2013 Jun;125(6):897–908.
  • Rivest S. Regulation of innate immune responses in the brain. Nat Rev Immunol. 2009 Jun;9(6):429–439.
  • Hu G, Yao H, Chaudhuri AD, et al. Exosome-mediated shuttling of microRNA-29 regulates HIV Tat and morphine-mediated neuronal dysfunction. Cell Death Dis. 2012 Aug 31;3:e381.
  • Yelamanchili SV, Lamberty BG, Rennard DA, et al. MiR-21 in extracellular vesicles leads to neurotoxicity via TLR7 signaling in SIV neurological disease. Douek DC, editor. PLoS Pathog. 2015 Jul;11(7):e1005032.
  • Klase Z, Kale P, Winograd R, et al. HIV-1 TAR element is processed by Dicer to yield a viral micro-RNA involved in chromatin remodeling of the viral LTR. BMC Mol Biol. 2007 Aug 01;8:63.
  • Raymond AD, Diaz P, Chevelon S, et al. Microglia-derived HIV Nef+ exosome impairment of the blood-brain barrier is treatable by nanomedicine-based delivery of Nef peptides. J Neurovirol. 2016 Apr;22(2):129–139.
  • Dominkuš PP, Ferdin J, Plemenitaš A, et al. Nef is secreted in exosomes from Nef.GFP-expressing and HIV-1-infected human astrocytes. J Neurovirol. 2017 Oct;23(5):713–724.
  • Sami Saribas A, Cicalese S, Ahooyi TM, et al. HIV-1 Nef is released in extracellular vesicles derived from astrocytes: evidence for Nef-mediated neurotoxicity. Cell Death Dis. 2017 Jan;8(1):e2542.
  • Khan MB, Lang MJ, Huang MB, et al. Nef exosomes isolated from the plasma of individuals with HIV-associated dementia (HAD) can induce Aβ1–42secretion in SH-SY5Y neural cells. J Neurovirol. 2016;22(2):179–190.
  • Rahimian P, He JJ. Exosome-associated release, uptake, and neurotoxicity of HIV-1 Tat protein. J Neurovirol. 2016 Dec;22(6):774–788.