Efficient infection, activation, and impairment of pDCs in the BM and peripheral lymphoid organs during early HIV-1 infection in humanized rag2 -/-γ C-/- mice in vivo

Blood

Volumn 117, Issue 23, 2011, Pages 6184-6192

  Zhang, Liguo ^a   Jiang, Qi ^b,c   Li, Guangming ^b   Jeffrey, Jerry ^b,c   Kovalev, Grigoriy I ^b   Su, Lishan ^a,b,c  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR;

ARTICLE; BONE MARROW; CD4+ T LYMPHOCYTE; CELL FUNCTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LYMPHOCYTE DEPLETION; LYMPHOID ORGAN; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; T LYMPHOCYTE ACTIVATION;

EID: 79959438765     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-01-331173     Document Type: Article

References (50)

1. Swiecki M, Gilfillan S, Vermi W, Wang Y, Colonna M. Plasmacytoid dendritic cell ablation impacts early interferon responses and antiviral NK and CD8(+) T cell accrual. Immunity. 2010; 33(6):955-966.
2. Colonna M, Trinchieri G, Liu YJ. Plasmacytoid dendritic cells in immunity. Nat Immunol. 2004; 5(12):1219-1226. (Pubitemid 41057736)
3. Liu YJ. IPC: professional type 1 interferonproducing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol. 2005;23:275-306.
4. Ito T, Wang YH, Liu YJ. Plasmacytoid dendritic cell precursors/type I interferon-producing cells sense viral infection by Toll-like receptor (TLR) 7 and TLR9. Springer Semin Immunopathol. 2005; 26(3):221-229.
5. Lande R, Gregorio J, Facchinetti V, et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature. 2007;449(7162): 564-569. (Pubitemid 47525141)
6. Cao W, Rosen DB, Ito T, et al. Plasmacytoid dendritic cell-specific receptor ILT7-Fc epsilonRI gamma inhibits Toll-like receptor-induced interferon production. J Exp Med. 2006;203(6):1399-1405. (Pubitemid 43877601)
7. Cao W, Bover L, Cho M, et al. Regulation of TLR7/9 responses in plasmacytoid dendritic cells by BST2 and ILT7 receptor interaction. J Exp Med. 2009;206(7):1603-1614.
8. 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(11):3265-3275. (Pubitemid 41567591)
9. Fonteneau JF, Larsson M, Beignon AS, et al. Human immunodeficiency virus type 1 activates plasmacytoid dendritic cells and concomitantly induces the bystander maturation of myeloid dendritic cells. J Virol. 2004;78(10):5223-5232. (Pubitemid 38581474)
10. Martinelli E, Cicala C, Van Ryk D, et al. HIV-1 gp120 inhibits TLR9-mediated activation and IFN-{alpha} secretion in plasmacytoid dendritic cells. Proc Natl Acad Sci U S A. 2007;104(9):3396-3401. (Pubitemid 46364170)
11. Perez-Caballero D, Zang T, Ebrahimi A, et al. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell. 2009;139(3):499-511.
12. Siegal FP, Kadowaki N, Shodell M, et al. The nature of the principal type 1 interferon-producing cells in human blood. Science. 1999;284(5421): 1835-1837.
13. Giorgi JV, Nishanian PG, Schmid I, Hultin LE, Cheng HL, Detels R. Selective alterations in immunoregulatory lymphocyte subsets in early HIV (human T-lymphotropic virus type III/lymphadenopathy-associated virus) infection. J Clin Immunol. 1987;7(2):140-150. (Pubitemid 17049973)
14. Siegal FP, Fitzgerald-Bocarsly P, Holland BK, Shodell M. Interferon-alpha generation and immune reconstitution during antiretroviral therapy for human immunodeficiency virus infection. Aids. 2001;15(13):1603-1612. (Pubitemid 32918114)
15. 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 RNA virus load. Blood. 2001;98(8):2574-2576.
16. 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(10):3016-3021.
17. 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(2):201-210.
18. Brown KN, Trichel A, Barratt-Boyes SM. Parallel loss of myeloid and plasmacytoid dendritic cells from blood and lymphoid tissue in simian AIDS. J Immunol. 2007;178(11):6958-6967. (Pubitemid 46847422)
19. Diop OM, Ploquin MJ, Mortara L, et al. Plasmacytoid dendritic cell dynamics and alpha interferon production during Simian immunodeficiency virus infection with a nonpathogenic outcome. J Virol. 2008;82(11):5145-5152. (Pubitemid 351705223)
20. 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(2):356-368. (Pubitemid 47223317)
21. Malleret B, Karlsson I, Maneglier B, et al. Effect of SIVmac infection on plasmacytoid and CD1c+ myeloid dendritic cells in cynomolgus macaques. Immunology. 2008;124(2):223-233. (Pubitemid 351692903)
22. Herbeuval JP, Shearer GM. HIV-1 immunopathogenesis: how good interferon turns bad. Clin Immunol. 2007;123(2):121-128. (Pubitemid 46590066)
23. Harris LD, Tabb B, Sodora DL, et al. 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. 2010;84(15):7886-7891.
24. Campillo-Gimenez L, Laforge M, Fay M, et al. 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. 2010;84(4):1838-1846.
25. Manches O, Bhardwaj N. Resolution of immune activation defines nonpathogenic SIV infection. J Clin Invest. 2009;119(12):3512-3515.
26. Jacquelin B, Mayau V, Targat B, et al. Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response. J Clin Invest. 2009;119(12):3544-3555.
27. Lederer S, Favre D, Walters KA, et al. Transcriptional profiling in pathogenic and non-pathogenic SIV infections reveals significant distinctions in kinetics and tissue compartmentalization. PLoS Pathog. 2009;5(2):e1000296.
28. Traggiai E, Chicha L, Mazzucchelli L, et al. Development of a human adaptive immune system in cord blood cell-transplanted mice. Science. 2004; 304(5667):104-107. (Pubitemid 38451466)
29. Shultz LD, Saito Y, Najima Y, et al. Generation of functional human T-cell subsets with HLArestricted immune responses in HLA class I expressing NOD/SCID/IL2r gamma(null) humanized mice. Proc Natl Acad Sci U S A. 2010; 107(29):13022-13027.
30. Strowig T, Gurer C, Ploss A, et al. Priming of protective T cell responses against virus-induced tumors in mice with human immune system components. J Exp Med. 2009;206(6):1423-1434.
31. Baenziger S, Tussiwand R, Schlaepfer E, et al. Disseminated and sustained HIV infection in CD34+ cord blood cell-transplanted Rag2-/-gamma c-/- mice. Proc Natl Acad Sci U S A. 2006; 103(43):15951-15956. (Pubitemid 44657573)
32. Jiang Q, Zhang L, Wang R, et al. FoxP3+CD4+ Treg cells play an important role in acute HIV-1 infection in humanized rag2-/-{gamma}C-/- mice in vivo. Blood. 2008;112(7):2858-2868.
33. Zhang L, Kovalev GI, Su L. HIV-1 infection and pathogenesis in a novel humanized mouse model. Blood. 2007;109(7):2978-2981. (Pubitemid 46482096)
34. Meissner EG, Coffield VM, Su L. Thymic pathogenicity of an HIV-1 envelope is associated with increased CXCR4 binding efficiency and V5-gp41-dependent activity, but not V1/V2-associated CD4 binding efficiency and viral entry. Virology. 2005;336(2):184-197. (Pubitemid 40693953)
35. Jamieson BD, Zack JA. In vivo pathogenesis of a human immunodeficiency virus type 1 reporter virus. J Virol. 1998;72(8):6520-6526. (Pubitemid 28323966)
36. Fong L, Mengozzi M, Abbey NW, Herndier BG, Engleman EG. Productive infection of plasmacytoid dendritic cells with human immunodeficiency virus type 1 is triggered by CD40 ligation. J Virol. 2002;76(21):11033-11041. (Pubitemid 35176220)
37. Yonezawa A, Morita R, Takaori-Kondo A, et al. Natural alpha interferon-producing cells respond to human immunodeficiency virus type 1 with alpha interferon production and maturation into dendritic cells. J Virol. 2003;77(6):3777-3784. (Pubitemid 36297296)
38. Smed-Sörensen A, Lore K, Vasudevan J, et al. Differential susceptibility to human immunodeficiency virus type 1 infection of myeloid and plasmacytoid dendritic cells. J Virol. 2005;79(14): 8861-8869. (Pubitemid 40934796)
39. Donaghy H, Gazzard B, Gotch F, Patterson S. Dysfunction and infection of freshly isolated blood myeloid and plasmacytoid dendritic cells in patients infected with HIV-1. Blood. 2003;101(11): 4505-4511. (Pubitemid 36857821)
40. Schmidt B, Scott I, Whitmore RG, et al. Low-level HIV infection of plasmacytoid dendritic cells: onset of cytopathic effects and cell death after PDC maturation. Virology. 2004;329(2):280-288. (Pubitemid 39423978)
41. Brown KN, Wijewardana V, Liu X, Barratt-Boyes SM. Rapid influx and death of plasmacytoid dendritic cells in lymph nodes mediate depletion in acute simian immunodeficiency virus infection. PLoS Pathog. 2009;5(5):e1000413.
42. Nascimbeni M, Perie L, Chorro L, et al. Plasmacytoid dendritic cells accumulate in spleens from chronically HIV-infected patients but barely participate in interferon-alpha expression. Blood. 2009;113(24):6112-6119.
43. Dillon SM, Robertson KB, Pan SC, et al. 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. 2008;48(1):1-12. (Pubitemid 351600852)
44. Lehmann C, Lafferty M, Garzino-Demo A, et al. Plasmacytoid dendritic cells accumulate and secrete interferon alpha in lymph nodes of HIV-1 patients. PLoS One. 2010;5(6):e11110.
45. Meyers JH, Justement JS, Hallahan CW, et al. Impact of HIV on cell survival and antiviral activity of plasmacytoid dendritic cells. PLoS ONE. 2007; 2(5):e458.
46. Howell DM, Feldman SB, Kloser P, Fitzgerald-Bocarsly P. Decreased frequency of functional natural interferon-producing cells in peripheral blood of patients with the acquired immune deficiency syndrome. Clin Immunol Immunopathol. 1994;71(2):223-230. (Pubitemid 24147241)
47. 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(8):3997-4006. (Pubitemid 351521235)
48. Sabado RL, O'Brien M, Subedi A, et al. Evidence of dysregulation of dendritic cells in primary HIV infection. Blood. 2010;116(19):3839-3852.
49. Meier A, Chang JJ, Chan ES, et al. Sex differences in the Toll-like receptor-mediated response of plasmacytoid dendritic cells to HIV-1. Nat Med. 2009;15(8):955-959.
50. Stary G, Klein I, Kohlhofer S, et al. Plasmacytoid dendritic cells express TRAIL and induce CD4+ T-cell apoptosis in HIV-1 viremic patients. Blood. 2009;114(18):3854-3863.