Abstract
Chimpanzees are susceptible to experimental infection by human deficiency virus (HIV)-1, but unlike humans, they exceptionally develop an immunodeficiency syndrome after HIV-1 inoculation. To explore the difference between human and chimpanzee, we analyzed the expression of 1547 genes of various functions in human or chimpanzee CD4+ lymphoblasts inoculated in vitro with HIV-1. We observed that, 1 day after HIV inoculation, fifty-eight genes were up-regulated in lymphoblasts of the three humans while their expression remained unchanged in lymphoblasts of the three chimpanzees. One gene is involved in adhesion of HIV (catenin-alpha), three in the immune response (semaphorin 4D, placental growth factor, IL-6), three in apoptosis (deleted in colorectal carcinoma, caspase 9 and FOXO1A). No difference between species was revealed for the expression of 373 genes related to glycosylation pathways. The in vitro human/chimpanzee comparison reveals new candidate genes up-regulated after inoculation with HIV-1 only in human lymphoblasts and which could be related to the higher sensitivity of human to HIV-induced AIDS.
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Adachi M, Hayami M, Kashiwagi N, Mizuta T, Ohta Y, Gill MJ, et al. Expression of Ley antigen in human immunodeficiency virus-infected human T cell lines and in peripheral lymphocytes of patients with acquired immune deficiency syndrome (AIDS) and AIDS-related complex (ARC). J Exp Med. 1988;167:323–31.
Arendrup M, Hansen JE, Clausen H, Nielsen C, Mathiesen LR, Nielsen JO. Antibody to histo-blood group A antigen neutralizes HIV produced by lymphocytes from blood group A donors but not from blood group B or O donors. Aids. 1991;5:441–4.
Audige A, Urosevic M, Schlaepfer E, Walker R, Powell D, Hallenberger S, et al. Anti-HIV state but not apoptosis depends on IFN signature in CD4+ T cells. J Immunol. 2006;177:6227–37.
Balzarini J. The alpha(1,2)-mannosidase I inhibitor 1-deoxymannojirimycin potentiates the antiviral activity of carbohydrate-binding agents against wild-type and mutant HIV-1 strains containing glycan deletions in gp120. FEBS Lett. 2007;581:2060–4.
Botarelli P, Houlden BA, Haigwood NL, Servis C, Montagna D, Abrignani S. N-glycosylation of HIV-gp120 may constrain recognition by T lymphocytes. J Immunol. 1991;147:3128–32.
Brass AL, Dykxhoorn DM, Benita Y, Yan N, Engelman A, Xavier RJ, et al. Identification of host proteins required for HIV infection through a functional genomic screen. Science. 2008;319:921–6.
Burt TD, Agan BK, Marconi VC, He W, Kulkarni H, Mold JE, Cavrois M, Huang Y, Mahley RW, Dolan MJ, McCune JM, Ahuja SK. Apolipoprotein (apo) E4 enhances HIV-1 cell entry in vitro, and the APOE epsilon4/epsilon4 genotype accelerates HIV disease progression. Proc Natl Acad Sci U S A. 2008;105:8718–23.
Bushman FD, Malani N, Fernandes J, D’Orso I, Cagney G, Diamond TL, et al. Host cell factors in HIV replication: meta-analysis of genome-wide studies. PLoS Pathog. 2009;5:e1000437.
Forcet C, Ye X, Granger L, Corset V, Shin H, Bredesen DE, et al. The dependence receptor DCC (deleted in colorectal cancer) defines an alternative mechanism for caspase activation. Proc Natl Acad Sci U S A. 2001;98:3416–21.
Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, et al. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature. 1999;397:436–41.
Gougeon ML, Lecoeur H, Boudet F, Ledru E, Marzabal S, Boullier S, et al. Lack of chronic immune activation in HIV-infected chimpanzees correlates with the resistance of T cells to Fas/Apo-1 (CD95)-induced apoptosis and preservation of a T helper 1 phenotype. J Immunol. 1997;158:2964–76.
Heeney J, Jonker R, Koornstra W, Dubbes R, Niphuis H, Di Rienzo AM, et al. The resistance of HIV-infected chimpanzees to progression to AIDS correlates with absence of HIV-related T-cell dysfunction. J Med Primatol. 1993;22:194–200.
Hiraiwa N, Hiraiwa M, Kannagi R. Human T-cell leukemia virus-1 encoded Tax protein transactivates alpha 1→3 fucosyltransferase Fuc-T VII, which synthesizes sialyl Lewis X, a selectin ligand expressed on adult T-cell leukemia cells. Biochem Biophys Res Commun. 1997;231:183–6.
Hodara VL, Parodi LM, Chavez D, Smith LM, Lanford R, Giavedoni LD. Characterization of γδT cells in naïve and HIV-infected chimpanzees and their responses to T-cell activators in vitro. J Med Primatol. 2014;43:258–71.
Hu H, Shioda T, Moriya C, Xin X, Hasan MK, Miyake K, et al. Infectivities of human and other primate lentiviruses are activated by desialylation of the virion surface. J Virol. 1996;70:7462–70.
Imbeault M, Ouellet M, Tremblay MJ. Microarray study reveals that HIV-1 induces rapid type-I interferon-dependent p53 mRNA up-regulation in human primary CD4+ T cells. Retrovirology. 2009;6:5.
Keele BF, Jones JH, Terio KA, Estes JD, Rudicell RS, Wilson ML, et al. Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature. 2009;460:515–9.
Kestens L, Vingerhoets J, Peeters M, Vanham G, Vereecken C, Penne G, et al. Phenotypic and functional parameters of cellular immunity in a chimpanzee with a naturally acquired simian immunodeficiency virus infection. J Infect Dis. 1995;172:957–63.
Kim N, Dabrowska A, Jenner RG, Aldovini A. Human and simian immunodeficiency virus-mediated upregulation of the apoptotic factor TRAIL occurs in antigen-presenting cells from AIDS-susceptible but not from AIDS-resistant species. J Virol. 2007;81:7584–97.
Kim JT, Kim EM, Lee KH, Choi JE, Jhun BH, Kim JW. Leucine zipper domain of HIV-1 gp41 interacted specifically with alpha-catenin. Biochem Biophys Res Commun. 2002;291:1239–44.
Kumanogoh A, Kikutani H. Immune semaphorins: a new area of semaphorin research. J Cell Sci. 2003;116:3463–70.
Lucque MC, Santos CC, Mairena EC, Wilkinson P, Boucher G, Segurado AC, Fonseca LA, Sabino E, Kalil JE, Cunha-Neto E. Gene expression profile in long-term non progressor HIV infected patients: in search of potential resistance factors. Mol Immunol. 2014;62:63–70.
Modur V, Nagarajan R, Evers BM, Milbrandt J. FOXO proteins regulate tumor necrosis factor-related apoptosis inducing ligand expression. Implications for PTEN mutation in prostate cancer. J Biol Chem. 2002;277:47928–37.
Ondoa P, Davis D, Kestens L, Vereecken C, Garcia Ribas S, Fransen K, et al. In vitro susceptibility to infection with SIVcpz and HIV-1 is lower in chimpanzee than in human peripheral blood mononuclear cells. J Med Virol. 2002;67:301–11.
O’Neil SP, Novembre FJ, Hill AB, Suwyn C, Hart CE, Evans-Strickfaden T, et al. Progressive infection in a subset of HIV-1-positive chimpanzees. J Infect Dis. 2000;182:1051–62.
Pandrea I, Apetrei C, Gordon S, Barbercheck J, Dufour J, Bohm R, et al. Paucity of CD4+CCR5+ T cells is a typical feature of natural SIV hosts. Blood. 2007;109:1069–76.
Peeters M, Janssens W, Vanden Haesevelde M, Fransen K, Willems B, Heyndrickx L, et al. Virologic and serologic characteristics of a natural chimpanzee lentivirus infection. Virology. 1995;211:312–5.
Pepe MG, Curtiss LK. Apolipoprotein E is a biologically active constituent of the normal immunoregulatory lipoprotein, LDL-In. J Immunol. 1986;136:3716–23.
Pollakis G, Kang S, Kliphuis A, Chalaby MI, Goudsmit J, Paxton WA. N-linked glycosylation of the HIV type-1 gp120 envelope glycoprotein as a major determinant of CCR5 and CXCR4 coreceptor utilization. J Biol Chem. 2001;276:13433–41.
Rotger M, Dalmau J, Rauch A, McLaren P, Bosinger SE, Martinez R, et al. Comparative transcriptomics of extreme phenotypes of human HIV-1 infection and SIV infection in sooty mangabey and rhesus macaque. J Clin Invest. 2011;121:2391–400.
Rutjens E, Balla-Jhagjhoorsingh S, Verschoor E, Bogers W, Koopman G, Heeney J. Lentivirus infections and mechanisms of disease resistance in chimpanzees. Front Biosci. 2003;8:d1134–45.
Schuitemaker H, Meyaard L, Kootstra NA, Dubbes R, Otto SA, Tersmette M, et al. Lack of T cell dysfunction and programmed cell death in human immunodeficiency virus type 1-infected chimpanzees correlates with absence of monocytotropic variants. J Infect Dis. 1993;168:1140–7.
Selvaraj SK, Giri RK, Perelman N, Johnson C, Malik P, Kalra VK. Mechanism of monocyte activation and expression of proinflammatory cytochemokines by placenta growth factor. Blood. 2003;102:1515–24.
Silvestri G, Paiardini M, Pandrea I, Lederman MM, Sodora DL. Understanding the benign nature of SIV infection in natural hosts. J Clin Invest. 2007;117:3148–54.
Stevenson M, Zhang XH, Volsky DJ. Downregulation of cell surface molecules during noncytopathic infection of T cells with human immunodeficiency virus. J Virol. 1987;61:3741–8.
Tordjman R, Lepelletier Y, Lemarchandel V, Cambot M, Gaulard P, Hermine O, et al. A neuronal receptor, neuropilin-1, is essential for the initiation of the primary immune response. Nat Immunol. 2002;3:477–82.
Trinite B, Chan CN, Lee CS, Mahajan S, Luo Y, Muesing MA, Folkvord JM, Pham M, Connick E, Levy DN. Suppression of Foxo1 activity and down-modulation of CD62L (L-selectin) in HIV-1 infected resting CD4 T cells. PLoS One. 2014;9(10):e110719.
Vahey MT, Nau ME, Jagodzinski LL, Yalley-Ogunro J, Taubman M, Michael NL, et al. Impact of viral infection on the gene expression profiles of proliferating normal human peripheral blood mononuclear cells infected with HIV type 1 RF. AIDS Res Hum Retrovir. 2002;18:179–92.
van ‘t Wout AB, Lehrman GK, Mikheeva SA, O’Keeffe GC, Katze MG, Bumgarner RE, et al. Cellular gene expression upon human immunodeficiency virus type 1 infection of CD4(+)-T-cell lines. J Virol. 2003;77:1392–402.
Viard JP, Burgard M, Hubert JB, Aaron L, Rabian C, Pertuiset N, et al. Impact of 5 years of maximally successful highly active antiretroviral therapy on CD4 cell count and HIV-1 DNA level. Aids. 2004;18:45–9.
Vigerust DJ, Shepherd VL. Virus glycosylation: role in virulence and immune interactions. Trends Microbiol. 2007;15:211–8.
Wen W, Chen S, Cao Y, Zhu Y, Yamamoto Y. HIV-1 infection initiates changes in the expression of a wide array of genes in U937 promonocytes and HUT78 T cells. Virus Res. 2005;113:26–35.
Zaitseva M, Lee S, Lapham C, Taffs R, King L, Romantseva T, et al. Interferon gamma and interleukin 6 modulate the susceptibility of macrophages to human immunodeficiency virus type 1 infection. Blood. 2000;96:3109–17.
Zhou H, Xu M, Huang Q, Gates AT, Zhang XD, Castle JC, et al. Genome-scale RNAi screen for host factors required for HIV replication. Cell Host Microbe. 2008;4:495–504.
Acknowledgments
This study was supported by the Ministère Français de la Recherche (Contract EA3034) and Association de Recherche sur le SIDA (A.R.S., Toulouse, France). We thank Christine Bousquet and Christine Taureau for their excellent technical assistance.
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Pol-André Apoil and Arnaud Gleizes have contributed equally to this work.
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Puissant-Lubrano, B., Apoil, PA., Gleizes, A. et al. Modulation of gene expression in CD4+ T lymphocytes following in vitro HIV infection: a comparison between human and chimpanzee. VirusDis. 26, 62–69 (2015). https://doi.org/10.1007/s13337-015-0252-1
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DOI: https://doi.org/10.1007/s13337-015-0252-1