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Inhibition of Infection and Transmission of HIV-1 and Lack of Significant J Antimicrob Chemother 2013; 68: 2026–2037 doi:10.1093/jac/dkt152 Advance Access publication 2 May 2013 Inhibition of infection and transmission of HIV-1 and lack of significant impact on the vaginal commensal lactobacilli by carbohydrate-binding agents Mariya I. Petrova1,2†, Leen Mathys3†, Sarah Lebeer1,2, Sam Noppen3, Els J. M. Van Damme4, Haruo Tanaka5, Yasuhiro Igarashi6, Mario Vaneechoutte7, Jos Vanderleyden1 and Jan Balzarini3* Downloaded from https://academic.oup.com/jac/article/68/9/2026/782524 by guest on 27 September 2021 1Centre of Microbial and Plant Genetics, KU Leuven, Kasteelpark Arenberg 20, bus 2460, B-3001 Leuven, Belgium; 2Department of Bioscience Engineering, University of Antwerp, Groenenborgerlaan 171, B-2020 Antwerp, Belgium; 3Rega Institute for Medical Research, KU Leuven, Minderbroedersstraat 10, B-3000 Leuven, Belgium; 4Laboratory of Biochemistry and Glycobiology, Department of Molecular Biotechnology, Ghent University, Coupure links 653, B-9000 Ghent, Belgium; 5Faculty of Pharmacy and College of Science and Engineering, Iwaki Meisei University, Iwaki, Fukushima 970-8551, Japan; 6Biotechnology Research Center, Toyama Prefectural University, Toyama 939-0398, Japan; 7Laboratory of Bacteriology Research, Ghent University, De Pintelaan 185, B-9000 Ghent, Belgium *Corresponding author. Tel: +32-16-337367; Fax: +32-16-337340; E-mail: [email protected] †These authors contributed equally to this work. Received 12 November 2012; returned 4 February 2013; revised 13 March 2013; accepted 25 March 2013 Objectives: A selection of carbohydrate-binding agents (CBAs) with different glycan specificities were evaluated for their inhibitory effect against HIV infection and transmission, and their interaction with vaginal commensal bacteria. Methods: Several assays were used for the antiviral evaluation: (i) cell-free virus infection of human CD4+ T lymphocyte C8166 cells; (ii) syncytium formation in co-cultures of persistently HIV-1-infected HUT-78/HIV-1 and non-infected CD4+ SupT1 cells; (iii) DC-SIGN-directed capture of HIV-1 particles; and (iv) transmission of DC-SIGN-captured HIV-1 particles to uninfected CD4+ C8166 cells. CBAs were also examined for their interaction with vaginal commensal lactobacilli using several viability, proliferation and adhesion assays. Results: The CBAs showed efficient inhibitory activity in the nanomolar to low-micromolar range against four events that play a crucial role in HIV-1 infection and transmission: cell-free virus infection, fusion between HIV- 1-infected and non-infected cells, HIV-1 capture by DC-SIGN and transmission of DC-SIGN-captured virus to T cells. As candidate microbicides should not interfere with the normal human microbiota, we examined the effect of CBAs against Lactobacillus strains, including a variety of vaginal strains, a gastrointestinal strain and several non-human isolates. None of the CBAs included in our studies inhibited the growth of these bacteria in several media, affected their viability or had any significant impact on their adhesion to HeLa cell monolayers. Conclusions: The CBAs in this study were inhibitory to HIV-1 in several in vitro infection and transmission models, and may therefore qualify as potential microbicide candidates. The lack of significant impact on commensal vaginal lactobacilli is an important property of these CBAs in view of their potential microbicidal use. Keywords: adhesion, HIV/AIDS, antimicrobial agents, antiretroviral therapy, bacterial biofilms, lactic acid bacteria, microbicides Introduction will result in the exposure of previously hidden immunogenic epi- Carbohydrate-binding agents (CBAs) comprise a broad and struc- topes to the immune system.1 A variety of CBAs derived from turally diverse functional class of agents, which may become the several organisms other than mammals have been described to first chemotherapeutics with a dual mechanism of antiviral be endowed with anti-HIV activity (for an overview, see Franc¸ois action: first, through direct antiviral activity by binding the and Balzarini2). Such CBAs include plant, invertebrate and prokary- glycans of the virus envelope and blocking virus entry, and otic lectins. The CBAs may qualify as potential microbicidal agents second, through indirect antiviral action by exerting pressure on since several among them have the intrinsic potential not only to the virus to select for deletions in the envelope glycan shield that inhibit virus infection and interaction between (gp120-expressing) # The Author 2013. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For Permissions, please e-mail: [email protected] 2026 Lack of toxicity of anti-HIV CBAs against vaginal lactobacilli JAC virus-infected cells and uninfected cells, but also to prevent the Test compounds used in this study capture of virus particles by dendritic cell-specific intercellular ad- The CBAs used in the study are shown in Table 1 together with their carbo- hesion molecule-3 grabbing non-integrin (DC-SIGN)-expressing hydrate specificities.11 – 16 The plant lectins derived from Galanthus nivalis + cells and subsequent transmission to uninfected CD4 T lympho- (GNA), Hippeastrum hybrid (HHA) and Urtica dioica agglutinin (UDA) were 1,2 cytes. However, when introducing these molecules as microbi- kindly provided by E. J. M. Van Damme (Ghent, Belgium).17,18 Actinohivin cides in complex hosts for prevention and/or therapy of viral (AH) prepared from a cultured broth of an actinomycete, Longispora infections, the CBAs will also come into contact with the normal albida K97-0003T was provided by H. Tanaka (Fukushima, Japan).19 Pradi- microbiota, which are important for the health of the host and micin A (PRM-A)20 and pradimicin S (PRM-S)21,22 were obtained from Profes- which should preferentially not be affected by the CBAs. Lactoba- sor T. Oki and Professor Y. Igarashi (Toyama, Japan). The monoclonal cilli are important beneficial members of the human vaginal and antibody 2G12 was purchased from Polymun Scientific (Vienna, Austria). gastrointestinal microbiota.3 It has been previously reported that lactobacilli have various carbohydrate-containing macromole- Downloaded from https://academic.oup.com/jac/article/68/9/2026/782524 by guest on 27 September 2021 4 –6 Viruses cules on their surface that might be possible targets for CBAs. The aim of this study was to evaluate and confirm the potential HIV-1NL4.3 was producedbythe simultaneoustransfection of HEK 293Tcells of several distinct CBAs to inhibit both infection and transmission of with a DNA construct encoding recombinant gp160 and XbaI-digested pNL4.3_DEnv_eGFP, which led to homologous recombination, thereby HIV in cell culture, and to investigate whether CBAs with promising 23 antiviral potential affect the growth, survival and adhesion cap- inserting the gp160 gene in the pNL4.3_eGFP backbone. As a result, acity of a broad variety of relevant (human) Lactobacillus strains. infected cells express enhanced green fluorescent protein (eGFP). The con- struct pNL4.3_DEnv_eGFP was kindly provided by Dr M. E. Quin˜ones-Mateu This study is therefore focusing on vaginal Lactobacillus species, (Lerner Research Institute, Cleveland, OH, USA).24 The produced wild-type since the vagina is the most important port of entry for HIV and virus was used to infect U87.CD4.CXCR4.CCR5, leading to an increased lactobacilli create a natural protection barrier in the human viral yield. vagina.6 –8 HIV-1IIIB was provided by R. C. Gallo and M. Popovic (Institute of Human Virology, University of Maryland, Baltimore, MD, at that time at the NIH, Materials and methods Bethesda, MD). Cell lines Bacteria Human CD4+ T lymphocytic C8166 and SupT1 cells were obtained from The bacterial strains, their origin and reference/source are shown in the ATCC (Manassas, VA, USA). HIV-1 -persistently infected Hut-78 cells IIIB Table 2.25 – 35 (Hut-78/HIV-1) were obtained after exposure of Hut-78 cells to wild-type HIV-1IIIB for 3–4 weeks. Human B-lymphocytic Raji/DC-SIGN cells, expres- sing DC-SIGN, were constructed by Geijtenbeek et al.9 and kindly provided by Dr L. Burleigh (Institut Pasteur, Paris, France). These cell lines were Antiretrovirus assays grownin RPMI-1640 medium(Invitrogen,Merelbeke, Belgium), supplemen- C8166 cells were grown in fresh culture medium (200 mL) in 96-well plates ted with 10% fetal calf serum (FCS) (Sigma, Bornem, Belgium), 2 mM at a density of 30000 cells/well. The appropriate concentrations of the test L-glutamine and 2% gentamicin (Invitrogen). compounds were added in 5-fold serial dilutions ranging between 20 mg/ Human embryonic kidney cells (HEK 293T) were obtained from the mL and 0.006 mg/mL. For flow cytometric analysis, wild-type HIV-1NL4.3 ATCC. U87.CD4.CCR5.CXCR4 cells were provided by Professor D. Schols was added at viral loads able to result in a 10% infection after 72 h. For (KU Leuven, Belgium) and their construction and characterization have scoring of the cytopathogenic effect (CPE), cells were infected with a viral 10 been described previously. Both cell lines were grown in Dulbecco’s load of 5-fold the CCID50, resulting in abundant giant cell formation after modified Eagle medium (DMEM) (Invitrogen), supplemented with 10% 72 h in the absence of the compounds. FCS (Sigma), 75 mM NaHCO3 and 2% gentamicin (Invitrogen). For the After 72 h of incubation at 378C, the cells were either microscopically U87.CD4.CXCR4.CCR5 cells, 1% puromycin (Invitrogen) and 0.02% geneti- examined for giant cell formation (CPE) or fixed in 3% formaldehyde for cin (Invitrogen) were added. flowcytometric analysis. The 50% effective concentration (EC50) wascalcu- Human cervix carcinoma HeLa cells were obtained from the ATCC. The lated asthe concentration of an agent required to suppress viral infection by cells were cultured at 378C in a 5% CO2/95% air atmosphere in DMEM 50%. Mutant HIV-1IIIB strains that had previously been isolated under CBA supplemented with 10% FCS. For the adhesion experiments, HeLa cells escalating selection conditions36,37 were also administered to C8166 cell were used at confluence, i.e. 4 days after seeding.
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