Primary infection with simian immunodeficiency virus: Plasmacytoid dendritic cell homing to lymph nodes, type I interferon, and immune suppression

Blood

Volumn 112, Issue 12, 2008, Pages 4598-4608

  Malleret, Benoît ^a,b   Manéglier, Benjamin ^c,d   Karlsson, Ingrid ^a,b   Lebon, Pierre ^e   Nascimbeni, Michelina ^f,g   Perié, Leïla ^f,g   Brochard, Patricia ^a,b   Delache, Benoît ^a,b   Calvo, Julien ^a,b   Andrieu, Thibault ^a,b   Spreux Varoquaux, Odile ^c,d   Hosmalin, Anne ^f,g   Le Grand, Roger ^a,b   Vaslin, Bruno ^a,b  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c UPRES EA 220   (France)

^d CENTRE HOSPITALIER DE VERSAILLES   (France)

^e Université Paris Descartes ^*  (France)

^f INSTITUT COCHIN   (France)

^g INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD123 ANTIGEN; CD20 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; INTERFERON; INTERLEUKIN 18; INTERLEUKIN 2 RECEPTOR ALPHA; TRANSCRIPTION FACTOR FOXP3;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BLOOD SAMPLING; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COUNT; CELL HOMING; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENZYME ACTIVITY; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOPATHOGENESIS; IMMUNOREGULATION; INNATE IMMUNITY; INTERFERON PRODUCTION; LYMPH NODE; LYMPHOCYTE COUNT; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC INFILTRATION; LYMPHOID TISSUE; MACACA; MONKEY DISEASE; NATURAL KILLER CELL; NONHUMAN; PRIMARY INFECTION; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; VIREMIA; VIRUS IMMUNITY; VIRUS LOAD; VIRUS REPLICATION; ACUTE PHASE RESPONSE; ANIMAL; BLOOD; CELL MOTION; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIMIAN IMMUNODEFICIENCY VIRUS;

ACUTE-PHASE REACTION; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; DENDRITIC CELLS; IMMUNE TOLERANCE; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERFERON TYPE I; INTERLEUKIN-18; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LYMPH NODES; MACACA FASCICULARIS; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIREMIA;

EID: 58149380860     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-06-162651     Document Type: Article

References (75)

1. Liu YJ. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol. 2005;23:275-306.
2. Cella M, Jarrossay D, Facchetti F, et al. Plasma-cytoid monocytes migrate to inflamed lymph nodes and produce large amounts of type I interferon. Nat Med. 1999;5:919-923.
3. Yoneyama H, Matsuno K, Zhang Y, et al. Evidence for recruitment of plasmacytoid dendritic cell precursors to inflamed lymph nodes through high endothelial venules. Int Immunol. 2004;16: 915-928.
4. Feldman S, Stein D, Amrute S, et al. Decreased interferon-alpha production in HIV-infected patients correlates with numerical and functional deficiencies in circulating type 2 dendritic cell precursors. Clin Immunol. 2001;101:201-210.
5. Pacanowski J, Kahi S, Baillet M, et al. Reduced blood CD123+ (lymphoid) and CD11c+ (myeloid) dendritic cell numbers in primary HIV-1 infection. Blood. 2001;98:3016-3021.
6. Soumelis V, Scott I, Gheyas F, et al. Depletion of circulating natural type 1 interferon-producing cells in HIV-infected AIDS patients. Blood. 2001; 98:906-912.
7. Ferbas JJ, Toso JF, Logar AJ, Navratil JS, Rinaldo CR, Jr. CD4+ blood dendritic cells are potent producers of IFN-alpha in response to in vitro HIV-1 infection. J Immunol. 1994;152:4649-4662.
8. Chehimi J, Campbell DE, Azzoni L, et al. Persistent decreases in blood plasmacytoid dendritic cell number and function despite effective highly active antiretroviral therapy and increased blood myeloid dendritic cells in HIV-infected individuals. J Immunol. 2002;168:4796-4801.
9. Barron MA, Blyveis N, Palmer BE, MaWhinney S, Wilson CC. Influence of plasma viremia on defects in number and immunophenotype of blood dendritic cell subsets in human immunodeficiency virus 1-infected individuals. J Infect Dis. 2003; 187:26-37.
10. Donaghy H, Pozniak A, Gazzard B, et al. Loss of blood CD11c(+) myeloid and CD11c(-) plasmacytoid dendritic cells in patients with HIV-1 infection correlates with HIV-1 RNAvirus load. Blood. 2001;98:2574-2576.
11. Finke JS, Shodell M, Shah K, Siegal FP, Steinman RM. Dendritic cell numbers in the blood of HIV-1 infected patients before and after changes in antiretroviral therapy. J Clin Immunol. 2004;24:647-652.
12. Schmidt B, Fujimura SH, Martin JN, Levy JA. Variations in plasmacytoid dendritic cell (PDC) and myeloid dendritic cell (MDC) levels in HIV-infected subjects on and off antiretroviral therapy. J Clin Immunol. 2006;26:55-64.
13. Almeida M, Cordero M, Almeida J, Orfao A. Different subsets of peripheral blood dendritic cells show distinct phenotypic and functional abnormalities in HIV-1 infection. Aids. 2005;19:261-271.
14. Foussat A, Bouchet-Delbos L, Berrebi D, et al. Deregulation of the expression of the fractalkine/ fractalkine receptor complex in HIV-1-infected patients. Blood. 2001;98:1678-1686.
15. Khatissian E, Tovey MG, Cumont MC, et al. The relationship between the interferon alpha response and viral burden in primary SIV infection. AIDS Res Hum Retroviruses. 1996;12:1273-1278.
16. Abel K, Alegria-Hartman MJ, Rothaeusler K, Marthas M, Miller CJ.The relationship between simian immunodeficiency virus RNA levels and the mRNA levels of alpha/beta interferons (IFN-alpha/beta) and IFN-alpha/beta-inducible Mx in lymphoid tissues of rhesus macaques during acute and chronic infection. J Virol. 2002;76: 8433-8445.
17. Giavedoni LD, Velasquillo MC, Parodi LM, Hubbard GB, HodaraVL. Cytokine expression, natural killer cell activation, and phenotypic changes in lymphoid cells from rhesus macaques during acute infection with pathogenic simian immunodeficiency virus. J Virol. 2000;74:1648-1657.
18. TeleshovaN, Kenney J, Jones J, et al. 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. 2004;173:1647-1657.
19. Reeves RK, Fultz PN. Disparate effects of acute and chronic infection with SIVmac239 or SHIV-89.6P on macaque plasmacytoid dendritic cells. Virology. 2007;365:356-368.
20. Beignon AS, McKenna K, Skoberne M, et al. Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J Clin Invest. 2005;115:3265-3275.
21. Boasso A, Herbeuval JP, Hardy AW, et al. HIV inhibits CD4+ T-cell proliferation by inducing indoleamine 2,3-dioxygenase in plasmacytoid dendritic cells. Blood. 2007;109:3351-3359.
22. Brown KN,TrichelA, Barratt-Boyes SM. Parallel loss of myeloid and plasmacytoid dendritic cells from blood and lymphoid tissue in simian AIDS. J Immunol. 2007;178:6958-6967.
23. Servet C, Zitvogel L, Hosmalin A. Dendritic cells in innate immune responses against HIV. Curr Mol Med. 2002;2:739-756.
24. Malleret B, Karlsson I, Manéglier B, et al. Effect of SIVmac infection on plasmacytoid and CD1c+ myeloid dendritic cells in cynomolgus macaques. Immunology. 2008;124:223-233.
25. Ozaki Y, Edelstein MP, Duch DS. Induction of indoleamine 2,3-dioxygenase: a mechanism of the antitumor activity of interferon gamma. Proc Natl Acad Sci U S A. 1988;85:1242-1246.
26. Mellor AL, Munn DH. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol. 2004;4:762-774.
27. Capuron L, Neurauter G, Musselman DL, et al. Interferon-alpha-induced changes in tryptophan metabolism. relationship to depression and paroxetine treatment. Biol Psychiatry. 2003;54:906-914.
28. Werner ER, Werner-Felmayer G, Fuchs D, HausenA, Reibnegger G, Wachter H. Effect of interferon gamma on tryptophan and pteridine metabolism of human cells. J Natl Cancer Inst. 1988;80:974-975.
29. Boasso A, Vaccari M, Hryniewicz A, et al. Regulatory T cell markers, indoleamine 2,3-dioxygenase, and virus levels in spleen and gut during progressive SIV infection. J Virol. 2007;81:11593-11603.
30. Estes JD, Li Q, Reynolds MR, et al. Premature induction of an immunosuppressive regulatory T cell response during acute simian immunodeficiency virus infection. J Infect Dis. 2006;193:703-712.
31. Fallarino F, Gizzi S, Mosci P, Grohmann U, Puccetti P. Tryptophan catabolism in IDO+ plasmacytoid dendritic cells. Curr Drug Metab. 2007; 8:209-216.
32. Benlhassan-Chahour K, Penit C, Dioszeghy V, et al. Kinetics of lymphocyte proliferation during primary immune response in macaques infected with pathogenic simian immunodeficiency virus SIVmac251: preliminary report of the effect of early antiviral therapy. J Virol. 2003;77:12479-12493.
33. Karlsson I, Malleret B, Brochard P, et al. FoxP3 + CD25 + CD8+ T-cell induction during primary SIV infection in cynomolgus macaques correlates with low CD4+ T-cell activation and high viral load. J Virol. 2007;81:13444-13455.
34. Maneglier B, Rogez-Kreuz C, Cordonnier P, et al. Simultaneous measurement of kynurenine and tryptophan in human plasma and supernatants of cultured human cells by HPLC with coulometric detection. Clin Chem. 2004;50:2166-2168.
35. Huengsberg M, Winer JB, Gompels M, Round R, Ross J, Shahmanesh M. Serum kynurenine-to-tryptophan ratio increases with progressive disease in HIV-infected patients. Clin Chem. 1998; 44:858-862.
36. Ankel H, Westra DF, Welling-Wester S, Lebon P. Induction of interferon-alpha by glycoprotein D of herpes simplex virus: a possible role of chemokine receptors. Virology. 1998;251:317-326.
37. Nakamura K, Okamura H, Nagata K, Komatsu T TamuraT. Purification of a factor which provides a costimulatory signal for gamma interferon production. Infect Immun. 1993;61:64-70.
38. Okamura H, Tsutsi H, Komatsu T, et al. Cloning of a new cytokine that induces IFN-gamma production by T cells. Nature. 1995;378:88-91.
39. Kaser A, Kaser S, Kaneider NC, Enrich B, Wiedermann CJ,Tilg H. Interleukin-18 attracts plasmacytoid dendritic cells (DC2s) and promotes Th1 induction by DC2s through IL-18 receptor expression. Blood. 2004;103:648-655.
40. Murray MF. Tryptophan depletion and HIV infection: a metabolic link to pathogenesis. Lancet Infect Dis. 2003;3:644-652.
41. ItoT, Kanzler H, Duramad O, Cao W, Liu YJ. Specialization, kinetics, and repertoire of type 1 interferon responses by human plasmacytoid predendritic cells. Blood. 2006;107:2423-2431.
42. Tilton JC, Manion MM, Luskin MR, et al. Human immunodeficiency virus viremia induces plasmacytoid dendritic cell activation in vivo and diminished alpha interferon production in vitro. J Virol. 2008;82:3997-4006.
43. Siegal FP, Kadowaki N, Shodell M, et al. The nature of the principal type 1 interferon-producing cells in human blood. Science. 1999;284:1835-1837.
44. Coates PT, Barratt-Boyes SM, Zhang L, et al. Dendritic cell subsets in blood and lymphoid tissue of rhesus monkeys and their mobilization with Flt3 ligand. Blood. 2003;102:2513-2521.
45. Kamga I, Kahi S, Develioglu L, et al. Type I interferon production is profoundly and transiently impaired in primary HIV-1 infection. J Infect Dis. 2005;192:303-310.
46. Karlsson I, Malleret B, Brochard P, et al. Dynamics of T cell responses and memory T cells during primary SIV infection in cynomolgus macaques. J Virol. 2007;81:13456-13468.
47. Sharma MD, Baban B, Chandler P, et al. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase. J Clin Invest. 2007;117:2570-2582.
48. Shortman K, Naik SH. Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol. 2007;7:19-30.
49. Merad M, Collin M, Bromberg J. Dendritic cell homeostasis and trafficking in transplantation. Trends Immunol. 2007;28:353-359.
50. Lore K, Sonnerborg A, Brostrom C, et al. Accumulation of DC-SIGN + CD40+ dendritic cells with reduced CD80 and CD86 expression in lymphoid tissue during acute HIV-1 infection. Aids. 2002; 16:683-692.
51. Zimmer MI, LarreginaAT, Castillo CM, et al. Disrupted homeostasis of Langerhans cells and interdigitating dendritic cells in monkeys with AIDS. Blood. 2002;99:2859-2868.
52. Biancotto A, Grivel JC, Iglehart SJ, et al. Abnormal activation and cytokine spectra in lymph nodes of people chronically infected with HIV-1. Blood. 2007;109:4272-4279.
53. Pantaleo G, Graziosi C, Demarest JF, et al. HIV infection is active and progressive in lymphoid tissue during the clinically latent stage of disease. Nature. 1993;362:355-358.
54. Tenner-Racz K, Racz P, Bofill M, et al. HTLV-III/ LAV viral antigens in lymph nodes of homosexual men with persistent generalized lymphadenopathy and AIDS. Am J Pathol. 1986;123:9-15.
55. Choi YK, Fallert BA, Murphey-Corb MA, Reinhart TA. Simian immunodeficiency virus dramatically alters expression of homeostatic chemokines and dendritic cell markers during infection in vivo. Blood. 2003;101:1684-1691.
56. Hardy AW, Graham DR, Shearer GM, Herbeuval JP. HIV turns plasmacytoid dendritic cells (pDC) into TRAIL-expressing killer pDC and down-regulates HIVcoreceptors by Toll-like receptor 7-induced IFN-alpha. Proc Natl Acad Sci USA. 2007;104:17453-17458.
57. Cecchinato V, Tryniszewska E, MaZM, et al. Immune activation driven by CTLA-4 blockade augments viral replication at mucosal sites in simian immunodeficiency virus infection. J Immunol. 2008;180:5439-5447.
58. Smith DG, Guillemin GJ, Pemberton L, et al. Quinolinic acid is produced by macrophages stimulated by platelet activating factor, Nef and Tat. J Neurovirol. 2001;7:56-60.
59. Maneglier B, Rogez-Kreuz C, Spreux-Varoquaux O, et al. Comparative effects of two type I interferons, human IFN-alphaand ovine IFN-tau on indoleamine-2,3-dioxygenase in primary cultures of human macrophages. Fundam Clin Pharmacol. 2007;21:29-34.
60. Fuchs D, Moller AA, Reibnegger G, Stockle E, Werner ER, Wachter H. Decreased serum tryptophan in patients with HIV-1 infection correlates with increased serum neopterin and with neurologic/psychiatric symptoms. J Acquir Immune Defic Syndr. 1990;3:873-876.
61. Norris PJ, Pappalardo BL, Custer B, Spotts G, Hecht FM, Busch MP. Elevations in IL-10, TNF-alpha, and IFN-gamma from the earliest point of HIVType 1 infection. AIDS Res Hum Retroviruses. 2006;22:757-762.
62. Curti A, Pandolfi S, Valzasina B, et al. Modulation of tryptophan catabolism by human leukemic cells results in the conversion of CD25- into CD25+ T regulatory cells. Blood. 2007;109:2871-2877.
63. Levings MK, Sangregorio R, Galbiati F Squadrone S, de Waal Malefyt R, Roncarolo MG. IFN-alphaand IL-10 induce the differentiation of human type 1 T regulatory cells. J Immunol. 2001;166:5530-5539.
64. Moseman EA, Liang X, Dawson AJ, et al. Human plasmacytoid dendritic cells activated by CpG oligodeoxynucleotides induce the generation of CD4 + CD25+ regulatory Tcells. J Immunol. 2004;173:4433-4442.
65. Billerbeck E, Blum HE, Thimme R. Parallel expansion of human virus-specific FoxP3- effector memory and de novo-generated FoxP3+ regulatory CD8+ Tcells upon antigen recognition in vitro. J Immunol. 2007;179:1039-1048.
66. Bisikirska B, Colgan J, Luban J, Bluestone JA, Herold KC. TCR stimulation with modified anti-CD3 mAb expands CD8+ T cell population and induces CD8 + CD25+ Tregs. J Clin Invest. 2005; 115:2904-2913.
67. Cosmi L, Liotta F, Lazzeri E, et al. Human CD8+CD25+ thymocytes share phenotypic and functional features with CD4+CD25+ regulatory thymocytes. Blood. 2003;102:4107-4114.
68. Joosten SA, van Meijgaarden KE, Savage ND, et al. Identification of a human CD8+ regulatory T cell subset that mediates suppression through the chemokine CC chemokine ligand 4. Proc Natl Acad Sci U S A. 2007;104:8029-8034.
69. Gavin MA, Torgerson TR, Houston E, et al. Single-cell analysis of normal and FOXP3-mutant human T cells: FOXP3 expression without regulatory T cell development. Proc Natl Acad Sci USA. 2006;103:6659-6664.
70. Chawla-Sarkar M, Lindner DJ, Liu YF, et al. Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis. 2003;8:237-249.
71. Frumento G, Rotondo R, Tonetti M, Damonte G, Benatti U, Ferrara GB. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J Exp Med. 2002; 196:459-468.
72. Gauduin MC, Yu Y, BarabaszA, et al. Induction of a virus-specific effector-memory CD4+ Tcell response by attenuated SIV infection. J Exp Med. 2006;203:2661-2672.
73. Benveniste O, Vaslin B, Le Grand R, et al. Comparative interleukin (IL-2)/interferon IFN-gamma and IL-4/IL-10 responses during acute infection of macaques inoculated with attenuated neftruncated or pathogenic SICmac251 virus. Proc Natl Acad Sci USA. 1996;93:3658-3663.
74. Robbins SH, Bessou G, Cornillon A, et al. Natural killer cells promote early CD8 T cell responses against cytomegalovirus. PLoS Pathog. 2007;3: e123.
75. Kadowaki N, Liu YJ. Natural type I interferon-producing cells as a link between innate and adaptive immunity. Hum Immunol. 2002;63:1126-1132.