Plasmacytoid Dendritic Cell Dynamics Tune Interferon-Alfa Production in SIV-Infected Cynomolgus Macaques

PLoS Pathogens

Volumn 10, Issue 1, 2014, Pages

  Bruel, Timothée ^a,b   Dupuy, Stéphanie ^a,b   Démoulins, Thomas ^a,b   Rogez Kreuz, Christine ^c   Dutrieux, Jacques ^d,e,f   Corneau, Aurélien ^a   Cosma, Antonio ^a,b   Cheynier, Rémi ^d,e,f   Dereuddre Bosquet, Nathalie ^a,b   Le Grand, Roger ^a,b   Vaslin, Bruno ^a,b  

^a CEA   (France)

^b INSTITUT D'OPTIQUE GRADUATE SCHOOL   (France)

^c Service of Neurovirology   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e INSTITUT COCHIN   (France)

^f CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 9;

ANIMAL; DENDRITIC CELL; IMMUNOLOGY; LYMPH NODE; MACACA FASCICULARIS; PATHOLOGY; PLASMA CELL; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS;

ANIMALS; DENDRITIC CELLS; INTERFERON-ALPHA; LYMPH NODES; MACACA FASCICULARIS; PLASMA CELLS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; TOLL-LIKE RECEPTOR 7; TOLL-LIKE RECEPTOR 9;

EID: 84893805677     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003915     Document Type: Article

References (51)

1. Douek DC, Roederer M, Koup RA, (2009) Emerging concepts in the immunopathogenesis of AIDS. Annu Rev Med 60: 471-484.
2. Chahroudi A, Bosinger SE, Vanderford TH, Paiardini M, Silvestri G, (2012) Natural SIV hosts: showing AIDS the door. Science 335: 1188-1193.
3. Bosinger SE, Li Q, Gordon SN, Klatt NR, Duan L, et al. (2009) Global genomic analysis reveals rapid control of a robust innate response in SIV-infected sooty mangabeys. J Clin Invest 119: 3556-3572.
4. Jacquelin B, Mayau V, Targat B, Liovat AS, Kunkel D, et al. (2009) Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response. J Clin Invest 119: 3544-3555.
5. Malleret B, Maneglier B, Karlsson I, Lebon P, Nascimbeni M, et al. (2008) Primary infection with simian immunodeficiency virus: plasmacytoid dendritic cell homing to lymph nodes, type I interferon, and immune suppression. Blood 112: 4598-4608.
6. Abel K, Rocke DM, Chohan B, Fritts L, Miller CJ, (2005) Temporal and anatomic relationship between virus replication and cytokine gene expression after vaginal simian immunodeficiency virus infection. J Virol 79: 12164-12172.
7. Easlick J, Szubin R, Lantz S, Baumgarth N, Abel K, (2010) The early interferon alpha subtype response in infant macaques infected orally with SIV. J Acquir Immune Defic Syndr 55: 14-28.
8. Abb J, (1987) Interferon-Alpha in Sera of Hiv-Infected Patients. Lancet 2: 1092-1093.
9. Campillo-Gimenez L, Laforge M, Fay M, Brussel A, Cumont MC, et al. (2010) Nonpathogenesis of simian immunodeficiency virus infection is associated with reduced inflammation and recruitment of plasmacytoid dendritic cells to lymph nodes, not to lack of an interferon type I response, during the acute phase. J Virol 84: 1838-1846.
10. Chehimi J, Papasavvas E, Tomescu C, Gekonge B, Abdulhaqq S, et al. (2010) Inability of plasmacytoid dendritic cells to directly lyse HIV-infected autologous CD4+ T cells despite induction of tumor necrosis factor-related apoptosis-inducing ligand. J Virol 84: 2762-2773.
11. Hughes R, Towers G, Noursadeghi M, (2012) Innate immune interferon responses to human immunodeficiency virus-1 infection. Rev Med Virol 22: 257-266.
12. Gilliet M, Cao W, Liu YJ, (2008) Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat Rev Immunol 8: 594-606.
13. Colonna M, Trinchieri G, Liu YJ, (2004) Plasmacytoid dendritic cells in immunity. Nat Immunol 5: 1219-1226.
14. Fonteneau JF, Larsson M, Beignon AS, McKenna K, Dasilva I, et al. (2004) Human immunodeficiency virus type 1 activates plasmacytoid dendritic cells and concomitantly induces the bystander maturation of myeloid dendritic cells. J Virol 78: 5223-5232.
15. Teleshova N, Kenney J, Jones J, Marshall J, Van Nest G, et al. (2004) CpG-C immunostimulatory oligodeoxyribonucleotide activation of plasmacytoid dendritic cells in rhesus macaques to augment the activation of IFN-gamma-secreting simian immunodeficiency virus-specific T cells. J Immunol 173: 1647-1657.
16. Beignon AS, McKenna K, Skoberne M, Manches O, DaSilva I, et al. (2005) Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J Clin Invest 115: 3265-3275.
17. Mandl JN, Barry AP, Vanderford TH, Kozyr N, Chavan R, et al. (2008) Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections. Nat Med 14: 1077-1087.
18. Li Q, Estes JD, Schlievert PM, Duan L, Brosnahan AJ, et al. (2009) Glycerol monolaurate prevents mucosal SIV transmission. Nature 458: 1034-1038.
19. Harris LD, Tabb B, Sodora DL, Paiardini M, Klatt NR, et al. (2010) Downregulation of robust acute type I interferon responses distinguishes nonpathogenic simian immunodeficiency virus (SIV) infection of natural hosts from pathogenic SIV infection of rhesus macaques. J Virol 84: 7886-7891.
20. Lehmann C, Harper JM, Taubert D, Hartmann P, Fatkenheuer G, et al. (2008) Increased interferon alpha expression in circulating plasmacytoid dendritic cells of HIV-1-infected patients. J Acquir Immune Defic Syndr 48: 522-530.
21. Lehmann C, Lafferty M, Garzino-Demo A, Jung N, Hartmann P, et al. (2010) Plasmacytoid dendritic cells accumulate and secrete interferon alpha in lymph nodes of HIV-1 patients. PLoS One 5: e11110.
22. Lehmann C, Taubert D, Jung N, Fatkenheuer G, van Lunzen J, et al. (2009) Preferential upregulation of interferon-alpha subtype 2 expression in HIV-1 patients. AIDS Res Hum Retroviruses 25: 577-581.
23. Nascimbeni M, Perie L, Chorro L, Diocou S, Kreitmann L, et al. (2009) Plasmacytoid dendritic cells accumulate in spleens from chronically HIV-infected patients but barely participate in interferon-alpha expression. Blood 113: 6112-6119.
24. Sabado RL, O'Brien M, Subedi A, Qin L, Hu N, et al. (2010) Evidence of dysregulation of dendritic cells in primary HIV infection. Blood 116: 3839-3852.
25. Geng W, Fan X, Diao Y, Cui H, Sun H, et al. (2011) Rapid disease progression in HIV-1-infected men who have sex with men is negatively correlated with peripheral plasmacytoid dendritic cell counts at the early stage of primary infection. J Clin Immunol 31: 882-890.
26. Cavaleiro R, Baptista AP, Soares RS, Tendeiro R, Foxall RB, et al. (2009) Major depletion of plasmacytoid dendritic cells in HIV-2 infection, an attenuated form of HIV disease. PLoS Pathog 5: e1000667.
27. Brown KN, Wijewardana V, Liu X, Barratt-Boyes SM, (2009) Rapid influx and death of plasmacytoid dendritic cells in lymph nodes mediate depletion in acute simian immunodeficiency virus infection. PLoS Pathog 5: e1000413.
28. Kwa S, Kannanganat S, Nigam P, Siddiqui M, Shetty RD, et al. (2011) Plasmacytoid dendritic cells are recruited to the colorectum and contribute to immune activation during pathogenic SIV infection in rhesus macaques. Blood 118: 2763-2773.
29. Reeves RK, Evans TI, Gillis J, Wong FE, Kang G, et al. (2012) SIV infection induces accumulation of plasmacytoid dendritic cells in the gut mucosa. J Infect Dis 206: 1462-1468.
30. Kamga I, Kahi S, Develioglu L, Lichtner M, Maranon C, et al. (2005) Type I interferon production is profoundly and transiently impaired in primary HIV-1 infection. J Infect Dis 192: 303-310.
31. Fitzgerald-Bocarsly P, Jacobs ES, (2010) Plasmacytoid dendritic cells in HIV infection: striking a delicate balance. J Leukoc Biol 87: 609-620.
32. Tilton JC, Manion MM, Luskin MR, Johnson AJ, Patamawenu AA, et al. (2008) Human immunodeficiency virus viremia induces plasmacytoid dendritic cell activation in vivo and diminished alpha interferon production in vitro. J Virol 82: 3997-4006.
33. O'Brien M, Manches O, Sabado RL, Baranda SJ, Wang Y, et al. (2011) Spatiotemporal trafficking of HIV in human plasmacytoid dendritic cells defines a persistently IFN-alpha-producing and partially matured phenotype. J Clin Invest 121: 1088-1101.
34. Kader M, Smith A, Guiducci C, Wonderlich E, Normolle D, et al. (2013) Blocking TLR7- and TLR9-mediated IFN-alpha production by plasmacytoid dendritic cells does not diminish immune activation in early SIV infection. Plos Pathogens 9 (7) (): e1003530.
35. Martin-Martin L, Almeida J, Hernandez-Campo PM, Sanchez ML, Lecrevisse Q, et al. (2009) Immunophenotypical, morphologic, and functional characterization of maturation-associated plasmacytoid dendritic cell subsets in normal adult human bone marrow. Transfusion 49: 1692-1708.
36. Reeves RK, Fultz PN, (2008) Characterization of plasmacytoid dendritic cells in bone marrow of pig-tailed macaques. Clin Vaccine Immunol 15: 35-41.
37. Ito T, Kanzler H, Duramad O, Cao W, Liu YJ, (2006) Specialization, kinetics, and repertoire of type 1 interferon responses by human plasmacytoid predendritic cells. Blood 107: 2423-2431.
38. Kitagawa M, Lackner AA, Martfeld DJ, Gardner MB, Dandekar S, (1991) Simian immunodeficiency virus infection of macaque bone marrow macrophages correlates with disease progression in vivo. Am J Pathol 138: 921-930.
39. Swiecki M, Wang Y, Vermi W, Gilfillan S, Schreiber RD, et al. (2011) Type I interferon negatively controls plasmacytoid dendritic cell numbers in vivo. J Exp Med 208: 2367-2374.
40. Mattei F, Bracci L, Tough DF, Belardelli F, Schiavoni G, (2009) Type I IFN regulate DC turnover in vivo. Eur J Immunol 39: 1807-1818.
41. Laforge M, Campillo-Gimenez L, Monceaux V, Cumont MC, Hurtrel B, et al. (2011) HIV/SIV Infection Primes Monocytes and Dendritic Cells for Apoptosis. Plos Pathogens 7: e1002087.
42. Dillon SM, Robertson KB, Pan SC, Mawhinney S, Meditz AL, et al. (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: 1-12.
43. Hoeffel G, Ripoche AC, Matheoud D, Nascimbeni M, Escriou N, et al. (2007) Antigen crosspresentation by human plasmacytoid dendritic cells. Immunity 27: 481-492.
44. Manches O, Fernandez MV, Plumas J, Chaperot L, Bhardwaj N, (2012) Activation of the noncanonical NF-kappaB pathway by HIV controls a dendritic cell immunoregulatory phenotype. Proc Natl Acad Sci U S A 109: 14122-14127.
45. Schmidt B, Ashlock BM, Foster H, Fujimura SH, Levy JA, (2005) HIV-infected cells are major inducers of plasmacytoid dendritic cell interferon production, maturation, and migration. Virology 343: 256-266.
46. Shacklett BL, Critchfield JW, Lemongello D, (2009) Isolating mucosal lymphocytes from biopsy tissue for cellular immunology assays. Methods Mol Biol 485: 347-356.
47. Malleret B, Karlsson I, Maneglier B, Brochard P, Delache B, et al. (2008) Effect of SIVmac infection on plasmacytoid and CD1c+ myeloid dendritic cells in cynomolgus macaques. Immunology 124: 223-233.
48. Roederer M, Nozzi JL, Nason MC, (2011) SPICE: exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A 79: 167-174.
49. Ankel H, Westra DF, Welling-Wester S, Lebon P, (1998) Induction of interferon-alpha by glycoprotein D of herpes simplex virus: a possible role of chemokine receptors. Virology 251: 317-326.
50. Karlsson I, Malleret B, Brochard P, Delache B, Calvo J, et al. (2007) Dynamics of T-cell responses and memory T cells during primary simian immunodeficiency virus infection in cynomolgus macaques. J Virol 81: 13456-13468.
51. Mannioui A, Bourry O, Sellier P, Delache B, Brochard P, et al. (2009) Dynamics of viral replication in blood and lymphoid tissues during SIVmac251 infection of macaques. Retrovirology 6: 106.