Cellular and Molecular Life Sciences

, Volume 75, Issue 10, pp 1871–1887 | Cite as

Early SIV and HIV infection promotes the LILRB2/MHC-I inhibitory axis in cDCs

  • Lamine Alaoui
  • Gustavo Palomino
  • Sandy Zurawski
  • Gerard Zurawski
  • Sixtine Coindre
  • Nathalie Dereuddre-Bosquet
  • Camille Lecuroux
  • Cecile Goujard
  • Bruno Vaslin
  • Christine Bourgeois
  • Pierre Roques
  • Roger Le Grand
  • Olivier Lambotte
  • Benoit FavierEmail author
Original Article


Classical dendritic cells (cDCs) play a pivotal role in the early events that tip the immune response toward persistence or viral control. In vitro studies indicate that HIV infection induces the dysregulation of cDCs through binding of the LILRB2 inhibitory receptor to its MHC-I ligands and the strength of this interaction was proposed to drive disease progression. However, the dynamics of the LILRB2/MHC-I inhibitory axis in cDCs during early immune responses against HIV are yet unknown. Here, we show that early HIV-1 infection induces a strong and simultaneous increase of LILRB2 and MHC-I expression on the surface of blood cDCs. We further characterized the early dynamics of LILRB2 and MHC-I expression by showing that SIVmac251 infection of macaques promotes coordinated up-regulation of LILRB2 and MHC-I on cDCs and monocytes/macrophages, from blood and lymph nodes. Orientation towards the LILRB2/MHC-I inhibitory axis starts from the first days of infection and is transiently induced in the entire cDC population in acute phase. Analysis of the factors involved indicates that HIV-1 replication, TLR7/8 triggering, and treatment by IL-10 or type I IFNs increase LILRB2 expression. Finally, enhancement of the LILRB2/MHC-I inhibitory axis is specific to HIV-1 and SIVmac251 infections, as expression of LILRB2 on cDCs decreased in naturally controlled chikungunya virus infection of macaques. Altogether, our data reveal a unique up-regulation of LILRB2 and its MHC-I ligands on cDCs in the early phase of SIV/HIV infection, which may account for immune dysregulation at a critical stage of the anti-viral response.


ILT4 HLA class I Immune checkpoint ITIM Innate immunity LILR SIRPa 



We thank the IDMIT infrastructure staff and Florian Meurisse for technical assistance. We also thank the ANRS cohorts CO6 PRIMO and CO21 CODEX for helpful collaboration and Anne Sophie Beignon for critical reading of the manuscript and helpful discussions. These works were supported by grants from the “Agence Nationale de Recherches sur le SIDA et les hépatites virales” under statement numbers 14-067, 16–035, University of Paris-Sud (Attractivité), European Union FP7 project (grant agreement no. 261202 (ICRES)), French government “Programme d’Investissements d’Avenir” (PIA) under Grant ANR-11-INBS-0008 funding the Infectious Disease Models and Innovative Therapies (IDMIT, Fontenay-aux-Roses, France) infrastructure and PIA grant ANR-10-EQPX-02-01 funding the FlowCyTech facility. G. Palomino was supported by a post-doctoral fellowship from Brazil government (Programa Ciência sem Fronteiras).

Supplementary material

18_2017_2712_MOESM1_ESM.eps (3.1 mb)
Figure S1. Generation and reactivity of anti-LILRB2 antibody (clone 17E5.3E9). (A) Amino acid sequence of human LILRB2 extracellular domain used to generate antibody 17E5.3E9. (B) Analysis of anti-LILRB2 antibody (clone 17E5.3E9) staining on cDCs, monocytes, neutrophils, eosinophils, CD4+ and CD8+ T cells, B cells and NK cells of healthy human and cynomolgus macaque blood samples. (C) Upregulation of LILRB2 is detected by 17E5.3E9 antibody on healthy human and cynomolgus macaque neutrophils stimulated with TNF-a. Flow cytometry analysis of LILRB2 at the surface of unstimulated (full line) or stimulated (dotted line) neutrophils for 30 min with TNF-a (100 ng/mL). Gray filled curve shows cells stained with isotype-matched control mAb. Data are representative of three independent experiments. (EPS 3132 kb)
18_2017_2712_MOESM2_ESM.eps (1.6 mb)
Figure S2. Flow cytometry gating strategy used to identify cell subsets of PBMCs from HIV-1+ patients. cDCs (CD1c+) were identified as Lin/HLA-DR+/CD16/CD14/CD123/CD11c+/CD1c+. Results shown are representative between individuals. (EPS 1685 kb)
18_2017_2712_MOESM3_ESM.eps (1.1 mb)
Figure S3. Characterization of HLA-DR expression level on cDCs during the early phase of HIV-1 infection. Analysis of HLA-DR surface expression on cDCs from blood samples of early HIV-1-infected patients before (primary HIV+) or after 1 year of cART (HIV+ cART+), HIV-1-infected elite controller patients (HIC), and HIV-1-non-infected controls (HIV-). Data are represented as mean fluorescence intensity with statistical analysis performed using the Mann–Whitney U test between HIC (n = 6), and primary HIV+ patients (n = 7) (p < 0,05 is considered significant). (EPS 1133 kb)
18_2017_2712_MOESM4_ESM.eps (2 mb)
Figure S4. Characterization of LILRB2 expression on immune cell subsets from secondary lymphoid organs of cynomolgus macaques. (A) Flow cytometry gating strategy used to identify cDCs and T and B cells of peripheral lymph nodes and spleen of cynomolgus macaques. cDCs were identified as CD45+/Lin(CD3/CD8/CD20)/HLA-DR+/CD163/CD123/CD1c+. (B) Flow cytometry analysis of LILRB2 expression on cDCs and on T and B cells from both peripheral and mesenteric lymph nodes, spleen, and peripheral blood (n = 4). (EPS 2019 kb)
18_2017_2712_MOESM5_ESM.eps (1.4 mb)
Figure S5. Follow-up of LILRB2 and MHC-I expression on monocytes and macrophages during infection of cynomolgus macaques by SIVmac251. (A) Monocyte cell counts during SIVmac251 infection, at 1000 AID50/mL, of 3 three female cynomolgus macaques. LILRB2 and MHC-I surface expression profiles of (B) blood monocytes and (C) lymph node macrophages. (D) Modulation of LILRB2 and MHC-I surface expression on blood monocytes from seven cynomolgus macaques followed at various time points during early (days 4 to 7, days 9 to 11, days 14 to 21, days 22 to 42) and advanced (days 57 to 100) phases of SIVmac251 infection. Data are shown as the fold change of surface expression relative to baseline (represented with dashed line). Statistical analyses were carried-out using the Wilcoxon matched-pairs signed rank test (p < 0.05 is considered significant). (EPS 1393 kb)
18_2017_2712_MOESM6_ESM.eps (1.3 mb)
Figure S6. Analysis of LILRB2 and MHC-I expression during SIV infection of three male cynomolgus macaques. (A) Plasma viral load of SIVmac251 infection at 1000 AID50/mL. (B) Modulation of LILRB2 (left panel) and MHC-I (right panel) expression on blood cDCs and (C) monocytes (CD14+/CD16). (D) Follow-up of LILRB2 surface expression on cDCs and macrophages isolated from peripheral lymph nodes of cynomolgus macaques during early (D + 14) and late (D + 85) phases of SIVmac251 infection. The surface expression of LILRB2 and MHC-I was determined by the mean fluorescence Intensity of each marker by flow cytometry. (EPS 1284 kb)
18_2017_2712_MOESM7_ESM.eps (1.1 mb)
Figure S7. Follow-up of SIRPa inhibitory receptor expression on cDCs during SIV infection of cynomolgus macaques. (A) Modulation of SIRPa expression on blood cDCs of three female cynomolgus macaques infected with 1000 AID50/mL of SIVmac251. (B) SIRPa expression on cDCs from secondary lymphoid tissue was evaluated from sampled peripheral lymph nodes at various time points after SIV infection. Data are represented as the mean Fluorescence Intensity. (EPS 1119 kb)
18_2017_2712_MOESM8_ESM.eps (1.1 mb)
Figure S8. Evolution of blood leucocyte counts during CHIKV infection of cynomolgus macaques. The evolution of cell counts of four cynomolgus macaques infected with the CHIKV-LR2006-OPY1 strain at a dose of 100 AID50/mL. (A) Follow-up of cDC counts analyzed by flow cytometry using Trucount tubes (BD biosciences). (B) Analysis of absolute blood cell numbers to follow the evolution of lymphocyte, monocyte, and granulocyte numbers using automated cell counts (HmX AL System, Beckman Coulter). (EPS 1111 kb)
18_2017_2712_MOESM9_ESM.eps (4.2 mb)
Figure S9. Schematic of LILRB2/MHC-I inhibitory axis regulation in cDCs of lymph nodes during HIV/SIV infection. (1) IL-10 and IFN-I stimulation along with HIV-1 sensing by TLR7/8 induce (2) the upregulation of LILRB2 expression allowing higher (3) Cis or Trans interactions with MHC-I ligands leading to (4) cDC dysfunctions. (EPS 4300 kb)
18_2017_2712_MOESM10_ESM.eps (1.2 mb)
Table S1. Monoclonal antibodies used for flow cytometry analysis of human and cynomolgus macaque samples. (EPS 1180 kb)


  1. 1.
    Merad M, Sathe P, Helft J, Miller J, Mortha A (2013) The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu Rev Immunol 31:563–604CrossRefPubMedGoogle Scholar
  2. 2.
    Steinman RM (2012) Decisions about dendritic cells: past, present, and future. Annu Rev Immunol 30:1–22CrossRefPubMedGoogle Scholar
  3. 3.
    Miller E, Bhardwaj N (2013) Dendritic cell dysregulation during HIV-1 infection. Immunol Rev 254:170–189CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Wijewardana V, Soloff AC, Liu X, Brown KN, Barratt-Boyes SM (2010) Early myeloid dendritic cell dysregulation is predictive of disease progression in simian immunodeficiency virus infection. PLoS Pathog 6:e1001235CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Wonderlich ER, Wu WC, Normolle DP, Barratt-Boyes SM (2015) Macrophages and myeloid dendritic cells lose T cell-stimulating function in simian immunodeficiency virus infection associated with diminished IL-12 and IFN-alpha production. J Immunol 195:3284–3292CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Chang CC, Ciubotariu R, Manavalan JS, Yuan J, Colovai AI, Piazza F, Lederman S, Colonna M, Cortesini R, Dalla-Favera R, Suciu-Foca N (2002) Tolerization of dendritic cells by T(S) cells: the crucial role of inhibitory receptors ILT3 and ILT4. Nat Immunol 3:237–243CrossRefPubMedGoogle Scholar
  7. 7.
    Lichterfeld M, Kavanagh DG, Williams KL, Moza B, Mui SK, Miura T, Sivamurthy R, Allgaier R, Pereyra F, Trocha A, Feeney M, Gandhi RT, Rosenberg ES, Altfeld M, Allen TM, Allen R, Walker BD, Sundberg EJ, Yu XG (2007) A viral CTL escape mutation leading to immunoglobulin-like transcript 4-mediated functional inhibition of myelomonocytic cells. J Exp Med 204:2813–2824CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Ristich V, Liang S, Zhang W, Wu J, Horuzsko A (2005) Tolerization of dendritic cells by HLA-G. Eur J Immunol 35:1133–1142CrossRefPubMedGoogle Scholar
  9. 9.
    Kang X, Kim J, Deng M, John S, Chen H, Wu G, Phan H, Zhang CC (2016) Inhibitory leukocyte immunoglobulin-like receptors: immune checkpoint proteins and tumor sustaining factors. Cell Cycle 15:25–40CrossRefPubMedGoogle Scholar
  10. 10.
    Colonna M, Samaridis J, Cella M, Angman L, Allen RL, O’Callaghan CA, Dunbar R, Ogg GS, Cerundolo V, Rolink A (1998) Human myelomonocytic cells express an inhibitory receptor for classical and nonclassical MHC class I molecules. J Immunol 160:3096–3100PubMedGoogle Scholar
  11. 11.
    Fanger NA, Cosman D, Peterson L, Braddy SC, Maliszewski CR, Borges L (1998) The MHC class I binding proteins LIR-1 and LIR-2 inhibit Fc receptor-mediated signaling in monocytes. Eur J Immunol 28:3423–3434CrossRefPubMedGoogle Scholar
  12. 12.
    Masuda A, Nakamura A, Maeda T, Sakamoto Y, Takai T (2007) Cis binding between inhibitory receptors and MHC class I can regulate mast cell activation. J Exp Med 204:907–920CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Mori Y, Tsuji S, Inui M, Sakamoto Y, Endo S, Ito Y, Fujimura S, Koga T, Nakamura A, Takayanagi H, Itoi E, Takai T (2008) Inhibitory immunoglobulin-like receptors LILRB and PIR-B negatively regulate osteoclast development. J Immunol 181:4742–4751CrossRefPubMedGoogle Scholar
  14. 14.
    Lichterfeld M, Yu XG (2012) The emerging role of leukocyte immunoglobulin-like receptors (LILRs) in HIV-1 infection. J Leukoc Biol 91:27–33CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Bashirova AA, Martin-Gayo E, Jones DC, Qi Y, Apps R, Gao X, Burke PS, Taylor CJ, Rogich J, Wolinsky S, Bream JH, Duggal P, Hussain S, Martinson J, Weintrob A, Kirk GD, Fellay J, Buchbinder SP, Goedert JJ, Deeks SG, Pereyra F, Trowsdale J, Lichterfeld M, Telenti A, Walker BD, Allen RL, Carrington M, Yu XG (2014) LILRB2 interaction with HLA class I correlates with control of HIV-1 infection. PLoS Genet 10:e1004196CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Huang J, Goedert JJ, Sundberg EJ, Cung TD, Burke PS, Martin MP, Preiss L, Lifson J, Lichterfeld M, Carrington M, Yu XG (2009) HLA-B*35-Px-mediated acceleration of HIV-1 infection by increased inhibitory immunoregulatory impulses. J Exp Med 206:2959–2966CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Jones DC, Kosmoliaptsis V, Apps R, Lapaque N, Smith I, Kono A, Chang C, Boyle LH, Taylor CJ, Trowsdale J, Allen RL (2011) HLA class I allelic sequence and conformation regulate leukocyte Ig-like receptor binding. J Immunol 186:2990–2997CrossRefPubMedGoogle Scholar
  18. 18.
    Sodora DL, Allan JS, Apetrei C, Brenchley JM, Douek DC, Else JG, Estes JD, Hahn BH, Hirsch VM, Kaur A, Kirchhoff F, Muller-Trutwin M, Pandrea I, Schmitz JE, Silvestri G (2009) Toward an AIDS vaccine: lessons from natural simian immunodeficiency virus infections of African nonhuman primate hosts. Nat Med 15:861–865CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Slukvin RL II, Grendell DS, Rao AL, Hughes, Golos TG (2006) “Cloning of rhesus monkey LILRs”. Tissue Antigens 67:331–337CrossRefPubMedGoogle Scholar
  20. 20.
    Labadie K, Larcher T, Joubert C, Mannioui A, Delache B, Brochard P, Guigand L, Dubreil L, Lebon P, Verrier B, de Lamballerie X, Suhrbier A, Cherel Y, Le Grand R, Roques P (2010) Chikungunya disease in nonhuman primates involves long-term viral persistence in macrophages. J Clin Invest 120:894–906CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Rougeron V, Sam IC, Caron M, Nkoghe D, Leroy E, Roques P (2015) Chikungunya, a paradigm of neglected tropical disease that emerged to be a new health global risk. J Clin Virol 64:144–152CrossRefPubMedGoogle Scholar
  22. 22.
    Banchereau J, Zurawski S, Thompson-Snipes L, Blanck JP, Clayton S, Munk A, Cao Y, Wang Z, Khandelwal S, Hu J, McCoy WHt, Palucka KA, Reiter Y, Fremont DH, Zurawski G, Colonna M, Shaw AS, Klechevsky E (2012) “Immunoglobulin-like transcript receptors on human dermal CD14+ dendritic cells act as a CD8-antagonist to control cytotoxic T cell priming”. Proc Natl Acad Sci USA 109:18885–18890CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Baudhuin J, Migraine J, Faivre V, Loumagne L, Lukaszewicz AC, Payen D, Favier B (2013) Exocytosis acts as a modulator of the ILT4-mediated inhibition of neutrophil functions. Proc Natl Acad Sci USA 110:17957–17962CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Maecker HT, Frey T, Nomura LE, Trotter J (2004) Selecting fluorochrome conjugates for maximum sensitivity. Cytometry A 62:169–173CrossRefPubMedGoogle Scholar
  25. 25.
    Huang J, Burke PS, Cung TD, Pereyra F, Toth I, Walker BD, Borges L, Lichterfeld M, Yu XG (2010) Leukocyte immunoglobulin-like receptors maintain unique antigen-presenting properties of circulating myeloid dendritic cells in HIV-1-infected elite controllers. J Virol 84:9463–9471CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Dillon SM, Robertson KB, Pan SC, Mawhinney S, Meditz AL, Folkvord JM, Connick E, McCarter MD, Wilson CC (2008) Plasmacytoid and myeloid dendritic cells with a partial activation phenotype accumulate in lymphoid tissue during asymptomatic chronic HIV-1 infection. J Acquir Immune Defic Syndr 48:1–12CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Sugimoto C, Hasegawa A, Saito Y, Fukuyo Y, Chiu KB, Cai Y, Breed MW, Mori K, Roy CJ, Lackner AA, Kim WK, Didier ES, Kuroda MJ (2015) Differentiation kinetics of blood monocytes and dendritic cells in macaques: insights to understanding human myeloid cell development. J Immunol 195:1774–1781CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Dutertre CA, Jourdain JP, Rancez M, Amraoui S, Fossum E, Bogen B, Sanchez C, Couedel-Courteille A, Richard Y, Dalod M, Feuillet V, Cheynier R, Hosmalin A (2014) TLR3-responsive, XCR1+, CD141(BDCA-3)+/CD8alpha+-equivalent dendritic cells uncovered in healthy and simian immunodeficiency virus-infected rhesus macaques. J Immunol 192:4697–4708CrossRefPubMedGoogle Scholar
  29. 29.
    Malleret B, Karlsson I, Maneglier B, Brochard P, Delache B, Andrieu T, Muller-Trutwin M, Beaumont T, McCune JM, Banchereau J, Le Grand R, Vaslin B (2008) Effect of SIVmac infection on plasmacytoid and CD1c+ myeloid dendritic cells in cynomolgus macaques. Immunology 124:223–233CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Wijewardana V, Kristoff J, Xu C, Ma D, Haret-Richter G, Stock JL, Policicchio BB, Mobley AD, Nusbaum R, Aamer H, Trichel A, Ribeiro RM, Apetrei C, Pandrea I (2013) Kinetics of myeloid dendritic cell trafficking and activation: impact on progressive, nonprogressive and controlled SIV infections. PLoS Pathog 9:e1003600CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Karlsson I, Malleret B, Brochard P, Delache B, Calvo J, Le Grand R, Vaslin B (2007) Dynamics of T-cell responses and memory T cells during primary simian immunodeficiency virus infection in cynomolgus macaques. J Virol 81:13456–13468CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Stacey AR, Norris PJ, Qin L, Haygreen EA, Taylor E, Heitman J, Lebedeva M, DeCamp A, Li D, Grove D, Self SG, Borrow P (2009) Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J Virol 83:3719–3733CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Addo MM, Altfeld M (2014) Sex-based differences in HIV type 1 pathogenesis. J Infect Dis 209(Suppl 3):S86–S92CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Saito Y, Iwamura H, Kaneko T, Ohnishi H, Murata Y, Okazawa H, Kanazawa Y, Sato-Hashimoto M, Kobayashi H, Oldenborg PA, Naito M, Kaneko Y, Nojima Y, Matozaki T (2010) Regulation by SIRPalpha of dendritic cell homeostasis in lymphoid tissues. Blood 116:3517–3525CrossRefPubMedGoogle Scholar
  35. 35.
    Le-Barillec K, Si-Tahar M, Balloy V, Chignard M (1999) Proteolysis of monocyte CD14 by human leukocyte elastase inhibits lipopolysaccharide-mediated cell activation. J Clin Invest 103:1039–1046CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Huang J, Al-Mozaini M, Rogich J, Carrington MF, Seiss K, Pereyra F, Lichterfeld M, Yu XG (2012) Systemic inhibition of myeloid dendritic cells by circulating HLA class I molecules in HIV-1 infection. Retrovirology 9:11CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Benlahrech A, Yasmin A, Westrop SJ, Coleman A, Herasimtschuk A, Page E, Kelleher P, Gotch F, Imami N, Patterson S (2012) Dysregulated immunophenotypic attributes of plasmacytoid but not myeloid dendritic cells in HIV-1 infected individuals in the absence of highly active anti-retroviral therapy. Clin Exp Immunol 170:212–221CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Huang J, Yang Y, Al-Mozaini M, Burke PS, Beamon J, Carrington MF, Seiss K, Rychert J, Rosenberg ES, Lichterfeld M, Yu XG (2011) Dendritic cell dysfunction during primary HIV-1 infection. J Infect Dis 204:1557–1562CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Favier B (2016) Regulation of neutrophil functions through inhibitory receptors: an emerging paradigm in health and disease. Immunol Rev 273:140–155CrossRefPubMedGoogle Scholar
  40. 40.
    Takai T (2005) A novel recognition system for MHC class I molecules constituted by PIR. Adv Immunol 88:161–192CrossRefPubMedGoogle Scholar
  41. 41.
    Wijewardana V, Bouwer AL, Brown KN, Liu X, Barratt-Boyes SM (2014) Accumulation of functionally immature myeloid dendritic cells in lymph nodes of rhesus macaques with acute pathogenic simian immunodeficiency virus infection. Immunology 143:146–154CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Barclay AN, Van den Berg TK (2014) The interaction between signal regulatory protein alpha (SIRPalpha) and CD47: structure, function, and therapeutic target. Annu Rev Immunol 32:25–50CrossRefPubMedGoogle Scholar
  43. 43.
    Guilliams M, Dutertre CA, Scott CL, McGovern N, Sichien D, Chakarov S, Van Gassen S, Chen J, Poidinger M, De Prijck S, Tavernier SJ, Low I, Irac SE, Mattar CN, Sumatoh HR, Low GH, Chung TJ, Chan DK, Tan KK, Hon TL, Fossum E, Bogen B, Choolani M, Chan JK, Larbi A, Luche H, Henri S, Saeys Y, Newell EW, Lambrecht BN, Malissen B, Ginhoux F (2016) Unsupervised high-dimensional analysis aligns dendritic cells across tissues and species. Immunity 45:669–684CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Laforge M, Campillo-Gimenez L, Monceaux V, Cumont MC, Hurtrel B, Corbeil J, Zaunders J, Elbim C, Estaquier J (2011) HIV/SIV infection primes monocytes and dendritic cells for apoptosis. PLoS Pathog 7:e1002087CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Roques P, Ljungberg K, Kummerer BM, Gosse L, Dereuddre-Bosquet N, Tchitchek N, Hallengard D, Garcia-Arriaza J, Meinke A, Esteban M, Merits A, Le Grand R, Liljestrom P (2017) Attenuated and vectored vaccines protect nonhuman primates against Chikungunya virus. JCI Insight 2:e83527CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Wauquier N, Becquart P, Nkoghe D, Padilla C, Ndjoyi-Mbiguino A, Leroy EM (2011) The acute phase of Chikungunya virus infection in humans is associated with strong innate immunity and T CD8 cell activation. J Infect Dis 204:115–123CrossRefPubMedGoogle Scholar
  47. 47.
    Schilte C, Couderc T, Chretien F, Sourisseau M, Gangneux N, Guivel-Benhassine F, Kraxner A, Tschopp J, Higgs S, Michault A, Arenzana-Seisdedos F, Colonna M, Peduto L, Schwartz O, Lecuit M, Albert ML (2010) Type I IFN controls chikungunya virus via its action on nonhematopoietic cells. J Exp Med 207:429–442CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  • Lamine Alaoui
    • 1
  • Gustavo Palomino
    • 1
  • Sandy Zurawski
    • 3
  • Gerard Zurawski
    • 3
  • Sixtine Coindre
    • 1
  • Nathalie Dereuddre-Bosquet
    • 1
  • Camille Lecuroux
    • 1
  • Cecile Goujard
    • 2
  • Bruno Vaslin
    • 1
  • Christine Bourgeois
    • 1
  • Pierre Roques
    • 1
  • Roger Le Grand
    • 1
  • Olivier Lambotte
    • 1
    • 2
  • Benoit Favier
    • 1
    Email author
  1. 1.CEA-Université Paris Sud 11-INSERM U1184, Immunology of Viral Infections and Autoimmune Diseases (IMVA), IDMIT Department, IBJF, DRFFontenay-aux-RosesFrance
  2. 2.Assistance Publique-Hôpitaux de Paris, Service de Médecine Interne et Immunologie Clinique, Groupe Hospitalier Universitaire Paris Sud, Hôpital BicêtreLe Kremlin-BicêtreFrance
  3. 3.Baylor Institute for Immunology ResearchDallasUSA

Personalised recommendations